Skip to main content

Advertisement

SpringerLink
Log in

Tracing of lipid markers of soft corals in a polar lipidome of the nudibranch mollusk Tritonia tetraquetra from the Sea of Okhotsk

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

To trace predator‒prey interactions in the marine environment, fatty acids (FAs) were widely applied as qualitative markers. Recently, two tetracosapolyenoic acids (TPA), which are specific markers of soft corals, have been found in the nudibranch mollusk Tritonia tetraquetra collected in the deep waters of the Sea of Okhotsk. This mollusk does not synthesize TPA but preys mostly on the soft coral Gersemia fruticosa. Both invertebrates are common species in Arctic and boreal regions and may be a simple model for the investigation of FA marker transfer from one trophic level to another. A lipidomic approach was applied to study the transfer of the FA markers in this predator–prey system. The structure and content of the molecular species of polar lipids (polar lipidome) of both animal species were analyzed by high-performance liquid chromatography with high-resolution tandem mass spectrometry. The distribution of several principal FA markers in lipid molecular species was determined. C20 monoenoic FAs of the coral were not integrated in the most of nudibranch lipids. Arachidonic and eicosapentaenoic acids mainly esterified ethanolamine and choline glycerophospholipids (PE and PC) in both invertebrates. In the coral polar lipidome, TPA concentrated in serine glycerophospholipids (PS). The nudibranch decomposed coral lipids and reallocated TPA to PS, PE, and PC. We suppose that this reallocation is responsible for the accumulation of TPA in the nudibranch. The nudibranch differed from the coral in biosynthetic relationships of phospholipid classes. The lipidomic approach explains the rearrangement of dietary FAs in the predator lipids. This rearrangement can be important for the trophic uptake and transfer of lipids in polar marine ecosystems.

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
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Auel H, Harjes M, da Rocha R, Stubing D, Hagen W (2002) Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biol 25:374–383

    Google Scholar 

  • Barnathan G (2009) Non-methylene-interrupted fatty acids from marine invertebrates: occurrence, characterization and biological properties. Biochimie 91:671–678

    Article  CAS  Google Scholar 

  • Beeman RD, Williams GC (1980) Opisthobranchia and pulmonata: the sea slugs and allies. In: Morris RH, Abbott DP, Haderlie EC (eds) Intertidal invertebrates of California. Stanford University Press, Stanford, pp 308–354

    Google Scholar 

  • Bishop DG, Kenrick JR (1980) Fatty acid composition of symbiotic zooxanthellae in relation to their hosts. Lipids 15:799–804

    Article  CAS  Google Scholar 

  • Blanchet-Aurigny A, Dubois SF, Quere C, Guillou M, Pernet F (2015) Trophic niche of two co-occurring ophiuroid species in impacted coastal systems, derived from fatty acid and stable isotope analyses. Mar Ecol Prog Ser 525:127–141. https://doi.org/10.3354/meps11169

    Article  CAS  Google Scholar 

  • Blom T, Somerharju P, Ikonen E (2011) Synthesis and biosynthetic trafficking of membrane lipids. Cold Spring Harb Perspect Biol 3:a004713

    Article  Google Scholar 

  • Boukhchina S, Seba K, Cherif A, Kallel H, Mayer PM (2004) Identification of glycerophospholipids in rapeseed, olive, almond, and sunflower oils by LC-MS and LC-MS-MS. Can J Chem 82:1210–1215

    Article  CAS  Google Scholar 

  • Braeckman U, Provoost P, Sabbe K, Soetaert K, Middelburg JJ, Vincx M, Vanaverbeke J (2015) Temporal dynamics in a shallow coastal benthic food web: insights from fatty acid biomarkers and their stable isotopes. Mar Environ Res 108:55–68

    Article  CAS  Google Scholar 

  • Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mam Sci 22:759–801

    Article  Google Scholar 

  • Calado R, Leal MC (2015) Trophic ecology of benthic marine invertebrates with bi-phasic life cycles: what are we still missing? Adv Mar Biol 71:1–70

    Article  Google Scholar 

  • Chen S, Belikova NA, Subbaiah PV (2012) Structural elucidation of molecular species of pacific oyster ether aminophospholipids by normal-phase liquid chromatography/negative-ion electrospray ionization and quadrupole/multiple-stage linear ion-trap mass spectrometry. Anal Chim Acta 735:76–89

    Article  CAS  Google Scholar 

  • Dalsgaard J, John MS, Kattner G, Muller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340

    Article  Google Scholar 

  • de Souza LM, Iacomini M, Gorin PAJ, Sari RS, Haddad MA, Sassaki GL (2007) Glyco- and sphingophosphonolipids from the medusa Phyllorhiza punctata: NMR and ESI-MS/MS fingerprints. Chem Phys Lipids 145:85–96

    Article  Google Scholar 

  • Drazen JC, Phleger CF, Guest MA, Nichols PD (2008) Lipid, sterols and fatty acid composition of abyssal holothurians and ophiuroids from the North-East Pacific Ocean: food web implications. Comp Biochem Physiol B 151:79–87

    Article  Google Scholar 

  • Fagone P, Jackowski S (2009) Membrane phospholipid synthesis and endoplasmic reticulum function. J Lipid Res 50:S311–S316

    Article  Google Scholar 

  • Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Garrett TA, Schmeitzel JL, Klein JA, Hwang JJ, Schwarz JA (2013) Comparative lipid profiling of the cnidarian Aiptasia pallida and its dinoflagellate symbiont. PLoS ONE 8:e57975

    Article  CAS  Google Scholar 

  • Graeve M, Kattner G, Piepenburg D (1997) Lipids in Arctic benthos: does the fatty acid and alcohol composition reflect feeding and trophic interactions? Polar Biol 18:53–61

    Article  Google Scholar 

  • Hamoutene D, Puestow T, Miller-Banoub J, Wareham V (2008) Main lipid classes in some species of deep-sea corals in the Newfoundland and Labrador region (Northwest Atlantic Ocean). Coral Reefs 27:237–246

    Article  Google Scholar 

  • Hanus LO, Levitsky DO, Shkrob I, Dembitsky VM (2009) Plasmalogens, fatty acids and alkyl glyceryl ethers of marine and freshwater clams and mussels. Food Chem 116:491–498

    Article  CAS  Google Scholar 

  • Hodson L, Murray Skeaff C, Fielding BA (2008) Fatty acid composition of adipose tissue and blood in humans and its use as a biomarker of dietary intake. Prog Lipid Res 47:348–380

    Article  CAS  Google Scholar 

  • Imbs AB (2016) High level of tetracosapolyenoic fatty acids in the cold-water mollusk Tochuina tetraquetra is a result of the nudibranch feeding on soft corals. Polar Biol 39:1511–1514

    Article  Google Scholar 

  • Imbs AB, Demina OA, Demidkova DA (2006) Lipid class and fatty acid composition of the boreal soft coral Gersemia rubiformis. Lipids 41:721–725

    Article  CAS  Google Scholar 

  • Imbs AB, Latyshev NA, Dautova TN, Latypov YY (2010) Distribution of lipids and fatty acids in corals by their taxonomic position and presence of zooxanthellae. Mar Ecol Prog Ser 409:65–75

    Article  CAS  Google Scholar 

  • Imbs AB, Dang LPT, Rybin VG, Nguyen NT, Pham LQ (2015a) Distribution of very-long-chain fatty acids between molecular species of different phospholipid classes of two soft corals. Biochem Anal Biochem 4:205

    Google Scholar 

  • Imbs AB, Dang LPT, Rybin VG, Svetashev VI (2015b) Fatty acid, lipid class, and phospholipid molecular species composition of the soft coral Xenia sp. (Nha Trang Bay, the South China Sea, Vietnam). Lipids 60:575–589

    Article  Google Scholar 

  • Imbs AB, Rybin VG, Kharlamenko VI, Dang LPT, Nguyen NT, Pham KM, Pham LQ (2015c) Polyunsaturated molecular species of galactolipids: markers of zooxanthellae in a symbiotic association of the soft coral Capnella sp. (Anthozoa: Alcyonacea). Russ J Mar Biol 41:461–467

    Article  CAS  Google Scholar 

  • Imbs AB, Demidkova DA, Dautova TN (2016) Lipids and fatty acids of cold-water soft corals and hydrocorals: a comparison with tropical species and implications for coral nutrition. Mar Biol 163:202

    Article  Google Scholar 

  • Jayasinghe C, Gotoh N, Wada S (2012) Regiospecific analysis of shark liver triacylglycerols. J Am Oil Chem Soc 89:1873–1884

    Article  CAS  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 

  • Kim H-Y, Huang BX, Spector AA (2014) Phosphatidylserine in the brain: metabolism and function. Prog Lipid Res 56:1–18

    Article  CAS  Google Scholar 

  • Kolts JM, Lovvorn JR, North CA, Grebmeier JM, Cooper LW (2013) Relative value of stomach contents, stable isotopes, and fatty acids as diet indicators for a dominant invertebrate predator (Chionoecetes opilio) in the northern Bering Sea. J Exp Mar Biol Ecol 449:274–283

    Article  CAS  Google Scholar 

  • Kraffe E, Soudant P, Marty Y (2004) Fatty acids of serine, ethanolamine, and choline plasmalogens in some marine bivalves. Lipids 39:59–66

    Article  CAS  Google Scholar 

  • Leal MC, Nunes C, Alexandre D, da Silva TL, Reis A, Dinis MT, Calado R (2012) Parental diets determine the embryonic fatty acid profile of the tropical nudibranch Aeolidiella stephanieae: the effect of eating bleached anemones. Mar Biol 159:1745–1751

    Article  CAS  Google Scholar 

  • Melo T, Alves E, Azevedo V, Martins AS, Neves D, Domingues P, Calado R, Abreu MH, Domingues MR (2015) Lipidomics as a new approach for the bioprospecting of marine macroalgae—unraveling the polar lipid and fatty acid composition of Chondrus crispus. Algal Res 8:181–191

    Article  Google Scholar 

  • Monroig O, Tocher DR, Navarro JC (2013) Biosynthesis of polyunsaturated fatty acids in marine invertebrates: recent advances in molecular mechanisms. Mar Drugs 11:3998–4018

    Article  Google Scholar 

  • Piccinetti CC, Ricci R, Pennesi C, Radaelli G, Totti C, Norici A, Giordano M, Olivotto I (2016) Herbivory in the soft coral Sinularia flexibilis (Alcyoniidae). Sci Rep 6:22679

    Article  CAS  Google Scholar 

  • Raphael W, Sordillo LM (2013) Dietary polyunsaturated fatty acids and inflammation: the role of phospholipid biosynthesis. Int J Mol Sci 14:21167–21188

    Article  Google Scholar 

  • Rybin VG, Imbs AB, Demidkova DA, Ermolenko EV (2017) Identification of molecular species of monoalkyldiacylglycerol from the squid Berryteuthis magister using liquid chromatography–APCI high-resolution mass spectrometry. Chem Phys Lipids 202:55–61

    Article  CAS  Google Scholar 

  • Saito H, Hashimoto J (2010) Characteristics of the fatty acid composition of a deep-sea vent gastropod, Ifremeria nautilei. Lipids 45:537–548

    Article  CAS  Google Scholar 

  • Spener F, Lagarde M, Geloen A, Record M (2003) What is lipidomics? Eur J Lipid Sci Tech 105:481–482

    Article  Google Scholar 

  • Svetashev VI (2011) Mild method for preparation of 4,4-dimethyloxazoline derivatives of polyunsaturated fatty acids for GC/MS. Lipids 46:463–467

    Article  CAS  Google Scholar 

  • Svetashev VI, Vysotskii MV (1998) Fatty acids of Heliopora coerulea and chemotaxonomic significance of tetracosapolyenoic acids in coelenterates. Comp Biochem Physiol B 119B:73–75

    Article  CAS  Google Scholar 

  • Tang CH, Ku PC, Lin CY, Chen TH, Lee KH, Lee SH, Wang WH (2015) Intra-colonial functional differentiation-related modulation of the cellular membrane in a pocilloporid coral Seriatopora caliendrum. Mar Biotechnol 17:633–643. https://doi.org/10.1007/s10126-015-9645-9

    Article  CAS  PubMed  Google Scholar 

  • The LipidWeb (2018) Mass spectrometry of fatty acid derivatives. http://www.lipidhome.co.uk/ms/masspec.html. Accessed 15 August 2018

  • Treignier C, Grover R, Ferrier-Pages C, Tolosa I (2008) Effect of light and feeding on the fatty acid and sterol composition of zooxanthellae and host tissue isolated from the scleractinian coral Turbinaria reniformis. Limnol Oceanogr 53:2702–2710

    Article  CAS  Google Scholar 

  • Vance JE (2008) Phosphatidylserine and phosphatidylethanolamine in mammalian cells: two metabolically related aminophospholipids. J Lipid Res 49:1377–1387

    Article  CAS  Google Scholar 

  • Vance JE, Steenbergen R (2005) Metabolism and functions of phosphatidylserine. Prog Lipid Res 44:207–234

    Article  CAS  Google Scholar 

  • Vance DE, Vance JE (2008) Phospholipid biosynthesis in eukaryotes. In: Vance DE, Vance JE (eds) Biochemistry of lipids, lipoproteins and membranes, 5th edn. Elsevier Science, Amsterdam, pp 215–244

    Google Scholar 

  • Vítová M, Goecke F, Sigler K, Řezanka T (2016) Lipidomic analysis of the extremophilic red alga Galdieria sulphuraria in response to changes in pH. Algal Res 13:218–226

    Article  Google Scholar 

  • Watson AD (2006) Lipidomics: a global approach to lipid analysis in biological systems. J Lipid Res 47:2101–2111

    Article  CAS  Google Scholar 

  • Wen B, Gao Q-F, Dong S-L, Hou Y-R, Yu H-B, Li W-D (2016) Uptake of benthic matter by sea cucumber Apostichopus japonicus (Selenka): Insights from carbon stable isotopes and fatty acid profiles. J Exp Mar Biol Ecol 474:46–53

    Article  CAS  Google Scholar 

  • Wessels H, Karsten U, Wiencke C, Hagen W (2012) On the potential of fatty acids as trophic markers in Arctic grazers: feeding experiments with sea urchins and amphipods fed nine diets of macroalgae. Polar Biol 35:555–565

    Article  Google Scholar 

  • Wicksten MK, DeMartini JD (1973) Observations of the feeding habits of Tochuina tetraquetra (Pallas) (Gastropoda: Tritoniidae). Veliger 15:195

    Google Scholar 

  • Zhu N, Dai X, Lin DS, Connor WE (1994) The lipids of slugs and snails: evolution, diet and biosynthesis. Lipids 29:869–875

    Article  CAS  Google Scholar 

  • Zhukova NV (2007) Lipid classes and fatty acid composition of the tropical nudibranch mollusks Chromodoris sp. and Phyllidia coelestis. Lipids 42:1169–1175

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Russian Foundation for Basic Research (Grant 15–04–02686). We thank Valeria P. Grigorchuk for her help with the LC–MS analysis and Dr. Vladimir I. Kharlamenko for collecting the biological materials and discussing the early versions of our manuscript. This manuscript benefited from valuable input by Prof. Dieter Piepenburg and three anonymous reviewers. Thanks are due to Evgenii P. Shvetsov for his help in improving the English.

Author information

Authors and Affiliations

  1. National Scientific Center of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, 17 Palchevskogo str, 690041, Vladivostok, Russian Federation

    Andrey B. Imbs & Alexei V. Chernyshev

Authors
  1. Andrey B. Imbs
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alexei V. Chernyshev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Andrey B. Imbs.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or vertebrate animals performed by any of the authors. All the experiments on invertebrate animals were reviewed and approved by the Ethics Committee of the National Scientific Center of Marine Biology, Far Eastern Branch of the Russian Academy of Sciences, and were conducted in agreement with the principles expressed in the Declaration of Helsinki.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 861 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Imbs, A.B., Chernyshev, A.V. Tracing of lipid markers of soft corals in a polar lipidome of the nudibranch mollusk Tritonia tetraquetra from the Sea of Okhotsk. Polar Biol 42, 245–256 (2019). https://doi.org/10.1007/s00300-018-2418-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-018-2418-y

Keywords

Search

Navigation