Advertisement

Genome-wide identification and expression of eight fatty acid desaturase genes, and the fatty acid profile, in the marine rotifer Brachionus koreanus fed the alga Tetraselmis suecica

  • Min-Chul Lee
  • Atsushi Hagiwara
  • Heum Gi Park
  • Jae-Seong LeeEmail author
Original Article Chemistry and Biochemistry

Abstract

Fatty acid desaturases catalyze the formation of a C=C double bond from a C–C single bond in fatty acids, leading to diversification of the fatty acid pool. In this study, we identified the fatty acid desaturase genes in the monogonont marine rotifer Brachionus koreanus, measured the messenger RNA (mRNA) expression, and quantified fatty acid composition under feeding with the alga Tetraselmis suecica. Eight fatty acid desaturase genes were identified and classified by phylogenetic analysis. Fatty acid desaturases in the rotifer B. koreanus were categorized into two Δ4 desaturases, five Δ5/6 desaturases, and one Δ9 desaturase. mRNA expression of B. koreanus under the alga T. suecica-fed condition clearly indicated that transcriptional levels of desaturase genes were increased compared to the non-T. suecica-fed group. Also, the distribution of fatty acids of B. koreanus fed T. suecica was more balanced compared to that of T. suecica. These results provide a better understanding of the role of fatty acid desaturases in B. koreanus fed the alga T. suecica.

Keywords

Fatty acid desaturase Tandem duplication Unsaturated fatty acid Phylogenetic analysis 

Notes

Acknowledgements

We thank two anonymous reviewers for their valuable comments that improved the manuscript. This work was supported by a grant from the National Research Foundation (2018R1D1A1B07050654) to Heum Gi Park.

Supplementary material

12562_2018_1286_MOESM1_ESM.docx (36 kb)
Supplementary material 1 (DOCX 36 kb)
12562_2018_1286_MOESM2_ESM.pptx (4.6 mb)
Supplementary material 2 (PPTX 4751 kb)

References

  1. Castro LFC, Tocher DR, Monroig Ó (2016) Long-chain polyunsaturated fatty acid biosynthesis in chordates: insights into the evolution of Fads and Elovl gene repertoire. Prog Lipid Res 62:25–40CrossRefGoogle Scholar
  2. Chen QM, Cheng DJ, Liu SP, Ma ZG, Tan X, Zhao P (2014) Genome-wide identification and expression profiling of the fatty acid desaturase gene family in the silkworm, Bombyx mori. Genet Mol Res 13:3747–3760CrossRefGoogle Scholar
  3. Cheng C, Geng F, Cheng X, Guo D (2018) Lipid metabolism reprogramming and its potential targets in cancer. Cancer Commun 38:27CrossRefGoogle Scholar
  4. Chertemps T, Duportets L, Labeur C, Ueyama M, Wicket-Thomas C (2006) A female-specific desaturase gene responsible for diene hydrocarbon biosynthesis and courtship behaviour in Drosophila melanogaster. Insect Mol Biol 15:465–473CrossRefGoogle Scholar
  5. Dahms H-U, Hagiwara A, Lee J-S (2011) Ecotoxicology, ecophysiology, and mechanistic studies with rotifers. Aquat Toxicol 17:1–12CrossRefGoogle Scholar
  6. Dallerac R, Labeur C, Jallon JM, Knipple DC, Roelofs WL, Wicker-Thomas C (2000) A delta 9 desaturase gene with a different substrate specificity is responsible for the cuticular diene hydrocarbon polymorphism in Drosophila melanogaster. Proc Natl Acad Sci USA 97:9449–9454CrossRefGoogle Scholar
  7. Dalsgaard J, St John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340CrossRefGoogle Scholar
  8. Gao QF, Shin PK, Lin GH, Chen SP, Cheung SG (2006) Stable isotope and fatty acid evidence for uptake organic waste by green-lipped mussels Perna viridis in a polyculture fish farm system. Mar Ecol Prog Ser 317:273–283CrossRefGoogle Scholar
  9. Gribble KE, Mark Welch DB (2017) Genome-wide transcriptomics of aging in the rotifer Brachionus manjavacas, an emerging model system. BMC Genom 18:217CrossRefGoogle Scholar
  10. Guillou H, Zadravec D, Marin PGP, Jacobsson A (2010) The key roles of elongases and desaturases in mammalian fatty acid metabolism: insights from transgenic mice. Prog Lipid Res 49:186–199CrossRefGoogle Scholar
  11. Gurr MI, Harwood JL, Frayn KN (2002) Lipid biochemistry. Blackwell Science, OxfordCrossRefGoogle Scholar
  12. Hama T, Handa N (1987) Pattern of organic matter production by natural phytoplankton population in a eutrophic lake. I. Intracellular products. Arch Hydrobiol 109:107–120Google Scholar
  13. Haritos VS, Horne I, Damcevski K, Glover K, Gibb N (2014) Unexpected functional diversity in the fatty acid desaturases of the flour beetle Tribolium castaneum and identification of key residues determining activity. Insect Biochem Mol Biol 51:62–70CrossRefGoogle Scholar
  14. Hastings N, Agaba M, Tocher DR, Leaver MJ, Dick JR, Sargent JR, Teale AJ (2001) A vertebrate fatty acid desaturase with delta 5 and delta 6 activities. Proc Natl Acad Sci USA 98:14304–14309CrossRefGoogle Scholar
  15. Holthuis JC, Menon AK (2014) Lipid landscapes and pipelines in membrane homeostasis. Nature 510:48–57CrossRefGoogle Scholar
  16. Horne I, Gibb N, Damcevski K, Glover K, Haritos VS (2010) Two conserved Z9-octadecanoic acid desaturases in the red flour beetle, Tribolium castaneum. Gene 468:41–47CrossRefGoogle Scholar
  17. Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307CrossRefGoogle Scholar
  18. Hwang D-S, Dahms H-U, Park HG, Lee J-S (2013) A new intertidal Brachionus and intrageneric phylogenetic relationships among Brachionus as revealed by allometry and CO1-ITS1 gene analysis. Zool Stud 52:1–10CrossRefGoogle Scholar
  19. Hwang D-S, Suga K, Sakakura Y, Park HG, Hagiwara A, Rhee J-S, Lee J-S (2014) Complete mitochondrial genome of the monogonont rotifer, Brachionus koreanus (Rotifera, Brachionidae). Mitochondrial DNA 25:29–30CrossRefGoogle Scholar
  20. Kabeya N, Chiba M, Haga Y, Satoh S, Yoshizaki G (2017) Cloning and functional characterization of fads2 desaturase and elovl5 elongase from Japanese flounder Paralichthys olivaceus. Comp Biochem Physiol B 214:36–46CrossRefGoogle Scholar
  21. Kabeya N, Fonseca MM, Ferrier DEK, Navarro JC, Bay LK, Francis DS, Tocher DR, Castro LFC, Monroig Ó (2018) Genes for de novo biosynthesis of omega-3 polyunsaturated fatty acids are widespread in animals. Sci Adv 4:eaar6849CrossRefGoogle Scholar
  22. Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22CrossRefGoogle Scholar
  23. Khotimchenko SV (2003) Fatty acids of species in the genus Codium. Bot Mar 46:456–460CrossRefGoogle Scholar
  24. Kim H-S, Han J, Kim H-J, Hagiwara A, Lee J-S (2017) Identification of 28 cytochrome P450 genes from the transcriptome of the marine rotifer Brachionus plicatilis and analysis of their expression. Comp Biochem Physiol D 23:1–7Google Scholar
  25. Lee J-S, Kim R-O, Rhee J-S, Han J, Hwang D-S, Choi B-S, Lee C-J, Yoon Y-D, Lim J-S, Lee Y-M, Park GS, Hagiwara A, Choi I-Y (2011) Sequence analysis of genomic DNA (680 Mb) by GS-FLX-titanium sequencer in the monogonont rotifer Brachionus ibericus. Hydrobiologia 662:65–75CrossRefGoogle Scholar
  26. Lee B-Y, Kim H-S, Hwang D-S, Won E-J, Choi B-S, Choi I-Y, Park HG, Rhee J-S, Lee J-S (2015) Whole transcriptome analysis of the monogonont rotifer Brachionus koreanus provides molecular resources for developing biomarkers of carbohydrate metabolism. Comp Biochem Physiol D 23:33–41Google Scholar
  27. Lee M-C, Han J, Lee S-H, Kim D-H, Kang H-M, Won E-J, Hwang D-S, Park JC, Om A-S, Lee J-S (2016a) A brominated flame retardant 2,2′,4,4′ tetrabrominated diphenyl ether (BDE-47) leads to lipogenesis in the copepod Tigriopus japonicus. Aquat Toxicol 178:19–26CrossRefGoogle Scholar
  28. Lee M-C, Puthumana J, Lee S-H, Kang H-M, Park JC, Jeong C-B, Han J, Hwang D-S, Seo JS, Park HG, Om A-S, Lee J-S (2016b) BDE-47 induces oxidative stress, activates MAPK signaling pathway, and elevates de novo lipogenesis in the copepod Paracyclopina nana. Aquat Toxicol 181:104–112CrossRefGoogle Scholar
  29. Lee M-C, Park JC, Kim D-H, Kang S, Shin K-H, Park H-G, Han J, Lee J-S (2017) Interrelationship of salinity shift with oxidative stress and lipid metabolism in the monogonont rotifer Brachionus koreanus. Comp Biochem Physiol A 214:79–84CrossRefGoogle Scholar
  30. Lee M-C, Park JC, Yoon D-S, Han J, Kang S, Kamizono S, Om A-S, Shin K-H, Hagiwara A, Lee J-S (2018) Aging extension and modification of lipid metabolism in the monogonont rotifer Brachionus koreanus under chronic caloric restriction. Sci Rep 29:1741CrossRefGoogle Scholar
  31. Lehane C, Davenport J (2002) Ingestion of mesozooplankton by three species of bivalve; Mytilus edulis, Cerastoderma edule and Aequipecten opercularis. J Mar Biol Assoc UK 82:615–619CrossRefGoogle Scholar
  32. Li J, Ding SF, Habib NA, Fermor BF, Wood CB, Gilmour RS (1994) Partial characterization of a cDNA for human stearoyl-CoA desaturase and changes in its mRNA expression in some normal and malignant tissues. Int J Cancer 57:348–352CrossRefGoogle Scholar
  33. Li X, Fan X, Han L, Lou Q (2002) Fatty acids of some algae from the Bohai Sea. Phytochemistry 59:157–161CrossRefGoogle Scholar
  34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefGoogle Scholar
  35. Marquardt A, Stohr H, White K, Weber BH (2000) cDNA cloning, genomic structure, and chromosomal localization of three members of the human fatty acid desaturase family. Genomics 66:175–183CrossRefGoogle Scholar
  36. Maxfield FR (2002) Plasma membrane microdomains. Curr Opin Cell Biol 14:483–487CrossRefGoogle Scholar
  37. Mills S, Alcántara-Rodríguez JA, Ciros-Pérez J, Gómez A, Hagiwara A, Galindo K, Jersabek CD, Malekzadeh-Viayeh R, Leasi F, Lee J-S, Mark Welch DB, Papakostas S, Riss S, Segers H, Serra M, Shiel R, Smolak R, Snell TW, Stelzer C-P, Tang CQ, Wallace RL, Fontaneto D, Walsh EJ (2017) Fifteen species in one: deciphering the Brachionus plicatilis species complex (Rotifera, Monogononta) through DNA taxonomy. Hydrobiologia 796:39–58CrossRefGoogle Scholar
  38. Monroig Ó, Kabeya N (2018) Desaturases and elongases involved in polyunsaturated fatty acid biosynthesis in aquatic invertebrates: a comprehensive review. Fish Sci 84:911–928CrossRefGoogle Scholar
  39. Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100:15682–15687CrossRefGoogle Scholar
  40. Mukherjee S, Maxfield FR (2004) Membrane domains. Annu Rev Cell Dev Biol 20:839–866CrossRefGoogle Scholar
  41. Nakamura MT, Nara TY (2004) Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 24:345–376CrossRefGoogle Scholar
  42. Park JC, Kim D-H, Lee M-C, Han J, Kim H-J, Hagiwara A, Hwang U-K, Park H-G, Lee J-S (2018) Genome-wide identification of the entire 90 glutathione S-transferase (GST) subfamily genes in four rotifer Brachionus species and transcriptional modulation in response to endocrine disrupting chemicals. Comp Biochem Physiol D 28:183–195Google Scholar
  43. Pomorski T, Hrafnsdottir S, Devaux DF, van Meer G (2001) Lipid distribution and transport across cellular membranes. Semin Cell Dev Biol 12:139–148CrossRefGoogle Scholar
  44. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: Advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. System Biol 63:793–808CrossRefGoogle Scholar
  45. Rodil IF, Olabarria C, Lastra M, López J (2008) Differential effects of native and invasive algal wrack on macrofaunal assemblages inhabiting exposed sandy beaches. J Exp Mar Biol Ecol 358:1–13CrossRefGoogle Scholar
  46. Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464CrossRefGoogle Scholar
  47. Segers H (2007) Annotated checklist of the rotifers (phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564:1–104Google Scholar
  48. Shanklin J, Cahoon EB (1998) Desaturation and related modifications of fatty acids. Annu Rev Plant Physiol Plant Mol Biol 49:611–641CrossRefGoogle Scholar
  49. Snell TW, Janssen CR (1995) Rotifers in ecotoxicology, a review. Hydrobiologia 313:231–247CrossRefGoogle Scholar
  50. Sperling P, Ternes P, Zank TK, Heinz E (2003) The evolution of desaturases. Prostagl Leukot Essent Fat Acids 68:73–95CrossRefGoogle Scholar
  51. Surm JM, Toledo TM, Prentis PJ, Pavasovic A (2018) Insights into the phylogenetic and molecular evolutionary histories of Fad and Elovl gene families in Actiniaria. Ecol Evol 00:1–13Google Scholar
  52. 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
  53. Tanomman S, Ketudat-Cairns M, Jangprai A, Boonanuntanasarn S (2013) Characterization of fatty acid-6 desaturase gene in Nile tilapia and heterogenous expression in Saccharomyces cerevisiae. Comp Biochem Physiol B 166:148–156CrossRefGoogle Scholar
  54. Thiede MA, Ozols J, Strittmatter P (1986) Construction and sequence of cDNA for rat liver stearyl coenzyme A desaturase. J Biol Chem 261:13230–13235Google Scholar
  55. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X Windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefGoogle Scholar
  56. Tocher DR, Leaver MJ, Hodgson PA (1998) Recent advances in the biochemistry and molecular biology of fatty acyl desaturases. Prog Lipid Res 37:73–117CrossRefGoogle Scholar
  57. van Meer G (2010) Membranes in motion. EMBO Rep 11:331–333CrossRefGoogle Scholar
  58. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124CrossRefGoogle Scholar
  59. Vaskovsky VE, Khotimchenko SV, Xia B, Li H (1996) Polar lipids and fatty acids of some marine macrophytes from the Yellow Sea. Phytochemistry 42:1347–1356CrossRefGoogle Scholar
  60. Wallace RL, Nogrady T, Snell TW, Ricci C (2006) Rotifera: biology, ecology and systematics (2nd ed.). Kenobi Productions, Belgium, Backhuys, the NetherlandsGoogle Scholar
  61. Wicker-Thomas C, Henriet C, Dallerac R (1997) Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochem Mol Biol 27:963–972CrossRefGoogle Scholar
  62. Zhu K, Choi KH, Schweizer HP, Rock CO, Zhang YM (2006) Two aerobic pathways for the formation of unsaturated fatty acids in Pseudomonas aeruginosa. Mol Microbiol 60:260–273CrossRefGoogle Scholar

Copyright information

© Japanese Society of Fisheries Science 2019

Authors and Affiliations

  1. 1.Department of Biological Science, College of ScienceSungkyunkwan UniversitySuwonSouth Korea
  2. 2.Graduate School of Fisheries and Environmental SciencesNagasaki UniversityNagasakiJapan
  3. 3.Organization for Marine Science and TechnologyNagasaki UniversityNagasakiJapan
  4. 4.Department of Marine Resource Development, College of Life SciencesGangneung-Wonju National UniversityGangneungSouth Korea

Personalised recommendations