Elsevier

Food Chemistry

Volume 265, 1 November 2018, Pages 49-56
Food Chemistry

Evaluation of lipid profile in different tissues of Japanese abalone Haliotis discus hannai Ino with UPLC-ESI-Q-TOF-MS-based lipidomic study

https://doi.org/10.1016/j.foodchem.2018.05.077Get rights and content

Highlights

Abstract

Abalone has been farmed commercially for the last few decades, and the breeding and economic value of abalone have gained extensive attention. In this study, the lipid profile of the foot muscles, viscera, and gonads of male and female Japanese abalone Haliotis discus hannai Ino was explored using ultra performance liquid chromatography-electrospray ionization-quadrupole time-of-flight mass spectrometry (UPLC-ESI-Q-TOF-MS), to discuss the effect of lipid composition on its nutritional value. Thirty-four species from ten lipid classes including phosphatidylcholine, phosphatidylethanolamine, phosphatidylserine, phosphatidylglycerol, phosphatidic acid, lysophosphatidic acid, triacylglycerol, steroids, terpenoids and fatty acids were annotated by MS-DIAL to obtain all fragment ions for precursors. Glycerophospholipids (GPLs) enriched in unsaturated fatty acids were the major components, which accounted for 52–57% of total lipids. Considering the high-level of GPLs, and their importance in maintaining the integrity and functionality of cell membranes, further utilization of inexpensive tissues, such as viscera and gonads is warranted.

Introduction

Japanese abalone Haliotis discus hannai Ino is a large algivorous marine mollusk (Mai, Wu, & Zhu, 2001). They are the main commercially-farmed species of abalone and have become the most important species of molluscan mariculture in Northern China, as they are high in commercial value among farmed molluscan products (Lou, Wang, & Xue, 2013). Traditionally, only the foot muscles of abalone were used for human consumption; viscera and gonad are mostly considered as by-products. Thus, in order to take advantage of these in a nutritional setting, more research is required on the lipid composition of different abalone tissues.

In abalone, over 75% of the tissue weight is water, with the remainder mostly composed of proteins, salts, lipids, and carbohydrates (Lou et al., 2013). Despite their low content, lipids are an indispensable component in abalone. Glycerophospholipids (GPLs) commonly present in abalone are a structural element of cell membranes and play a unique role in stabilizing cell membranes and protecting membrane lipids from hydrolytic enzymes (Mukhamedova & Glushenkova, 2000). Lipids play multiple critical roles in the cellular function of humans, such as composing the membrane bilayer, providing an appropriate hydrophobic environment for membrane proteins and their interactions, vesicle trafficking, secretion, and cytoskeletal rearrangement and participating in cell growth and multiplication (Harrison and Gadella, 2005, Hou et al., 2008). In addition to being essential structural and functional components of all cell membranes, GPLs, those mainly derived from diet, are being actively investigated for their role in human physiology and health. A recent study showed that the GPLs contributed to the formation of micelles in the intestinal lumen, via their role in biliary salts, in turn favoring the absorption of lipo-soluble molecules (Castro-Gómez, Garcia-Serrano, Visioli, & Fontecha, 2015). Studies focused on dairy products-derived GPLs indicated that consumption by adults could improve their cognitive function and memory (Crichton, Howe, Buckley, Coates, & Murphy, 2012).

With regards to lipidomics and lipid profiling, mass spectrometry is a powerful tool with high sensitivity and is primarily hyphenated to liquid chromatography or direct infusion (Xie, Zhong, Yu, & Chen, 2012). Direct infusion techniques were prevalent in the early stages of lipidomics research, due to their relative simplicity of operation, fast analysis, and the possibility to detect various lipid classes within a single run (Li et al., 2011, Loizides-Mangold, 2013). However, the popularity of LC-MS-based methods can be explained by several advantages over direct infusion techniques, including more reliable identification of individual lipid groups (even at trace levels), separation of isomers and isobars, and reduced ion-suppression effects. Also, current LC instruments allow more effective separation and reduce analysis time (Cajka and Fiehn, 2014, Lee et al., 2014). The direct injection of crude lipid extracts into ESI-MS could result in a significant loss of ion signals by ionization suppression of lipid groups from those low-abundance components (Hou et al., 2008, Jessome and Volmer, 2006). Fortunately, this problem can be avoided by the separation of lipids using chromatography. Time-of-flight mass spectrometry is among the top performers for this purpose, given its fast acquisition speed, superior sensitivity, high resolution, and excellent mass accuracy (Xie et al., 2012). In a metabolite identification study, the m/z (mass to charge ratio) of precursor and product ions are recorded in MS and MS/MS spectra, respectively, which provide crucial information for elemental composition analysis and structure elucidation (Zhu, Chen, & Subramanian, 2014).

Full-mass scanning followed by product ion, precursor ion (PI) and neutral loss (NL) scans has historically been the most common and comprehensive approach to identifying metabolites (Yin et al., 2016). However, these scan functions are relatively time-consuming and require repeat injections. Acquisition methods have evolved in the past years to minimize the need for multiple experiments, along with improved Q-TOF instruments to aid in metabolite screening and profiling. These methods are designed to either enable data-dependent acquisition (DDA) of targeted or non-targeted MS/MS spectra, or to generate pseudo-MS/MS datasets under the MSE acquisition mode, with the intention of identifying metabolites rapidly and straightforwardly from both in-vitro and in-vivo experiments (Xie et al., 2012).

The contents of unsaturated fatty acids in marine shellfish are very high. Abalone could provide ω-6 and ω-3 fatty acids for human nutrition. The compositions of fatty acids are very important for evaluation of the lipid profile in different tissues of abalone. However, LC-MS can only know the degree of unsaturation, and cannot get information about the location of the double bonds of fatty acids (Bird, Marur, Stavrovskaya, & Kristal, 2013). Therefore, the fatty acid chain structure of different lipid classes could only be determined by the combination of fatty acid esteration and gas chromatography-mass spectrometry.

In this study, the comprehensive characterization and semi-quantification of the lipid profile of different abalone tissues were conducted using ultra performance liquid chromatography-electrospray ionization-quadrupole time-of-flight mass spectrometry (UPLC-ESI-Q-TOF-MS), to facilitate the evaluation of the nutritional value of abalone. The molecular species were characterized according to MS and MS/MS spectra similarity matching to libraries from publicly-available databases with data-dependent MS/MS acquisition.

Section snippets

Materials

Fresh aquaculture Japanese abalone (Haliotis discus hannai Ino) were purchased from a local market in Dalian, China. To minimize the biological differences, thirty abalone were divided into three male groups and three female groups, each group containing five abalone. After removal of shells, fresh abalone tissues were separated into three parts: gonads, viscera and foot muscles. Different tissues from one group were homogenized and analyzed.

Chemicals

High-performance liquid chromatography (HPLC)-grade

UPLC-ESI-Q-TOF-MS analysis of abalone lipids

Over the past two decades, published research has addressed the lipid content of abalone, and the effects of abalone’s diet on its lipid content. To focus on health-benefiting n–3 long-chain polyunsaturated fatty acids, Mateos, Lewandowski, and Su (2010) examined fatty acid contents and composition in the muscles and gonads of farmed Jade Tiger hybrid abalone over four seasons. Other studies have expounded the influence of basic nutrient components such as carbohydrates on the lipid composition

Conclusions

The lipid profile, including lipid classes, FA compositions, and positions in lipids, as well as the content of each lipid group in abalone has been achieved by UPLC-ESI-Q-TOF-MS and annotated by MS-DIAL. PCA multivariate analysis was applied to analyze the various trends of lipid groups amongst different tissues of male and female abalone. The major functions of foot muscles are moving, with high requirement of a large amount of energy; the relatively low TG content detected in foot muscles

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31601432) and the National Key Research and Development Program of China (2016YFD0400404).

References (40)

  • N.Y. Schürer et al.

    Evidence for a novel keratinocyte fatty acid uptake mechanism with preference for linoleic acid: Comparison of oleic and linoleic acid uptake by cultured human keratinocytes, fibroblasts and a human hepatoma cell line

    Biochimica Et Biophysica Acta

    (1994)
  • H. Tapiero et al.

    Polyunsaturated fatty acids (PUFA) and eicosanoids in human health and pathologies

    Biomedecine & Pharmacotherapy

    (2002)
  • J.E. Vance

    Thematic review series: Glycerolipids. Phosphatidylserine and phosphatidylethanolamine in mammalian cells: Two metabolically related aminophospholipids

    Journal of Lipid Research

    (2008)
  • J.E. Vance et al.

    Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells

    Biochimica Et Biophysica Acta

    (2013)
  • X. Wang et al.

    Signaling functions of phosphatidic acid

    Progress in Lipid Research

    (2006)
  • X. Xu et al.

    Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (Rafts)

    Journal of Biological Chemistry

    (2001)
  • F.W. Yin et al.

    Identification of glycerophospholipid molecular species of mussel (Mytilus edulis) lipids by high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry

    Food Chemistry

    (2016)
  • S.S. Bird et al.

    Serum lipidomics profiling using LC-MS and high-energy collisional dissociation fragmentation: focus on triglyceride detection and characterization

    Analytical Chemistry

    (2011)
  • S.S. Bird et al.

    Qualitative characterization of the rat liver mitochondrial lipidome using LC-MS profiling and high energy collisional dissociation (HCD) all ion fragmentation

    Metabolomics

    (2013)
  • G.E. Crichton et al.

    Dairy consumption and cardiometabolic health: Outcomes of a 12-month crossover trial

    Nutrition & Metabolism

    (2012)
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