Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Chemistry and Biochemistry
  • Published:
Fisheries Science Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 62:25–40

    Article  CAS  PubMed  Google Scholar 

  • 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 13:3747–3760

    Article  CAS  PubMed  Google Scholar 

  • Cheng C, Geng F, Cheng X, Guo D (2018) Lipid metabolism reprogramming and its potential targets in cancer. Cancer Commun 38:27

    Article  Google Scholar 

  • 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 15:465–473

    Article  CAS  PubMed  Google Scholar 

  • Dahms H-U, Hagiwara A, Lee J-S (2011) Ecotoxicology, ecophysiology, and mechanistic studies with rotifers. Aquat Toxicol 17:1–12

    Article  CAS  Google Scholar 

  • 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 97:9449–9454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 46:225–340

    Article  PubMed  Google Scholar 

  • 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 317:273–283

    Article  CAS  Google Scholar 

  • Gribble KE, Mark Welch DB (2017) Genome-wide transcriptomics of aging in the rotifer Brachionus manjavacas, an emerging model system. BMC Genom 18:217

    Article  CAS  Google Scholar 

  • 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 49:186–199

    Article  CAS  PubMed  Google Scholar 

  • Gurr MI, Harwood JL, Frayn KN (2002) Lipid biochemistry. Blackwell Science, Oxford

    Book  Google Scholar 

  • Hama T, Handa N (1987) Pattern of organic matter production by natural phytoplankton population in a eutrophic lake. I. Intracellular products. Arch Hydrobiol 109:107–120

    CAS  Google Scholar 

  • 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 51:62–70

    Article  CAS  PubMed  Google Scholar 

  • 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 98:14304–14309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holthuis JC, Menon AK (2014) Lipid landscapes and pipelines in membrane homeostasis. Nature 510:48–57

    Article  CAS  PubMed  Google Scholar 

  • 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 468:41–47

    Article  CAS  PubMed  Google Scholar 

  • Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307

    Article  Google Scholar 

  • 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 52:1–10

    Article  CAS  Google Scholar 

  • 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 25:29–30

    Article  CAS  PubMed  Google Scholar 

  • 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 214:36–46

    Article  CAS  PubMed  Google Scholar 

  • 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:eaar6849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22

    Article  CAS  Google Scholar 

  • Khotimchenko SV (2003) Fatty acids of species in the genus Codium. Bot Mar 46:456–460

    Article  CAS  Google Scholar 

  • 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 23:1–7

    Google Scholar 

  • 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 662:65–75

    Article  CAS  Google Scholar 

  • 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 23:33–41

    Google Scholar 

  • 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 178:19–26

    Article  CAS  PubMed  Google Scholar 

  • 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 181:104–112

    Article  CAS  PubMed  Google Scholar 

  • 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 214:79–84

    Article  CAS  Google Scholar 

  • 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 29:1741

    Article  CAS  Google Scholar 

  • 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 82:615–619

    Article  Google Scholar 

  • 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 57:348–352

    Article  CAS  PubMed  Google Scholar 

  • Li X, Fan X, Han L, Lou Q (2002) Fatty acids of some algae from the Bohai Sea. Phytochemistry 59:157–161

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • 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 66:175–183

    Article  CAS  PubMed  Google Scholar 

  • Maxfield FR (2002) Plasma membrane microdomains. Curr Opin Cell Biol 14:483–487

    Article  CAS  PubMed  Google Scholar 

  • 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 796:39–58

    Article  CAS  Google Scholar 

  • Monroig Ó, Kabeya N (2018) Desaturases and elongases involved in polyunsaturated fatty acid biosynthesis in aquatic invertebrates: a comprehensive review. Fish Sci 84:911–928

    Article  CAS  Google Scholar 

  • Moore RC, Purugganan MD (2003) The early stages of duplicate gene evolution. Proc Natl Acad Sci USA 100:15682–15687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukherjee S, Maxfield FR (2004) Membrane domains. Annu Rev Cell Dev Biol 20:839–866

    Article  CAS  PubMed  Google Scholar 

  • Nakamura MT, Nara TY (2004) Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases. Annu Rev Nutr 24:345–376

    Article  CAS  PubMed  Google Scholar 

  • 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 28:183–195

    CAS  Google Scholar 

  • Pomorski T, Hrafnsdottir S, Devaux DF, van Meer G (2001) Lipid distribution and transport across cellular membranes. Semin Cell Dev Biol 12:139–148

    Article  CAS  PubMed  Google Scholar 

  • 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 63:793–808

    Article  Google Scholar 

  • 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 358:1–13

    Article  Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464

    Article  Google Scholar 

  • Segers H (2007) Annotated checklist of the rotifers (phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 1564:1–104

    Article  Google Scholar 

  • Shanklin J, Cahoon EB (1998) Desaturation and related modifications of fatty acids. Annu Rev Plant Physiol Plant Mol Biol 49:611–641

    Article  CAS  PubMed  Google Scholar 

  • Snell TW, Janssen CR (1995) Rotifers in ecotoxicology, a review. Hydrobiologia 313:231–247

    Article  Google Scholar 

  • Sperling P, Ternes P, Zank TK, Heinz E (2003) The evolution of desaturases. Prostagl Leukot Essent Fat Acids 68:73–95

    Article  CAS  Google Scholar 

  • 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 00:1–13

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 166:148–156

    Article  CAS  PubMed  Google Scholar 

  • Thiede MA, Ozols J, Strittmatter P (1986) Construction and sequence of cDNA for rat liver stearyl coenzyme A desaturase. J Biol Chem 261:13230–13235

    CAS  PubMed  Google Scholar 

  • 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 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tocher DR, Leaver MJ, Hodgson PA (1998) Recent advances in the biochemistry and molecular biology of fatty acyl desaturases. Prog Lipid Res 37:73–117

    Article  CAS  PubMed  Google Scholar 

  • van Meer G (2010) Membranes in motion. EMBO Rep 11:331–333

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Vaskovsky VE, Khotimchenko SV, Xia B, Li H (1996) Polar lipids and fatty acids of some marine macrophytes from the Yellow Sea. Phytochemistry 42:1347–1356

    Article  CAS  Google Scholar 

  • Wallace RL, Nogrady T, Snell TW, Ricci C (2006) Rotifera: biology, ecology and systematics (2nd ed.). Kenobi Productions, Belgium, Backhuys, the Netherlands

    Google Scholar 

  • Wicker-Thomas C, Henriet C, Dallerac R (1997) Partial characterization of a fatty acid desaturase gene in Drosophila melanogaster. Insect Biochem Mol Biol 27:963–972

    Article  CAS  PubMed  Google Scholar 

  • 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 60:260–273

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Biological Science, College of Science, Sungkyunkwan University, Suwon, 16419, South Korea

    Min-Chul Lee & Jae-Seong Lee

  2. Graduate School of Fisheries and Environmental Sciences, Nagasaki University, Nagasaki, 852-8521, Japan

    Atsushi Hagiwara

  3. Organization for Marine Science and Technology, Nagasaki University, Nagasaki, 852-8521, Japan

    Atsushi Hagiwara

  4. Department of Marine Resource Development, College of Life Sciences, Gangneung-Wonju National University, Gangneung, 25457, South Korea

    Heum Gi Park

Authors
  1. Min-Chul Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Atsushi Hagiwara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heum Gi Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jae-Seong Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jae-Seong Lee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 36 kb)

Supplementary material 2 (PPTX 4751 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, MC., Hagiwara, A., Park, H.G. et al. 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. Fish Sci 85, 397–406 (2019). https://doi.org/10.1007/s12562-018-01286-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-018-01286-9

Keywords

Search

Navigation