Evaluation of lipid profile in different tissues of Japanese abalone Haliotis discus hannai Ino with UPLC-ESI-Q-TOF-MS-based lipidomic study
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)
- et al.
Phosphatidylcholine biosynthesis and its significance in bacteria interacting with eukaryotic cells
European Journal of Cell Biology
(2010) - et al.
Comprehensive analysis of lipids in biological systems by liquid chromatography-mass spectrometry
Trends in Analytical Chemistry
(2014) - et al.
Relevance of dietary glycerophospholipids and sphingolipids to human health
Prostaglandins, Leukotrienes and Essential Fatty Acids (PLEFA)
(2015) - et al.
Ultra high performance liquid chromatography as a tool for the discovery and the analysis of biomarkers of diseases: A review
Journal of Chromatography B
(2013) - et al.
Lipid composition of Ruditapes philippinarum spat: Effect of ration and diet quality
Comparative Biochemistry & Physiology Part B
(2006) - et al.
A simple method for the isolation and purification of total lipides from animal tissues
Journal of Biological Chemistry
(1957) - et al.
Quantitative determination of phospholipid compositions by ESI-MS: Effects of acyl chain length, unsaturation, and lipid concentration on instrument response
Journal of Lipid Research
(2001) - et al.
Abalone, Haliotis discus hannai Ino, can synthesize myo-inositol de novo to meet physiological needs
Journal of Nutrition
(2001) - et al.
Seasonal variations of total lipid and fatty acid contents in muscle, gonad and digestive glands of farmed Jade Tiger hybrid abalone in Australia
Food Chemistry
(2010) - et al.
Characteristics of lipid and fatty acid of marine gastropod Turbo cornutus: High levels of arachidonic and n-3 docosapentaenoic acid
Food Chemistry
(2014)
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
Polyunsaturated fatty acids (PUFA) and eicosanoids in human health and pathologies
Biomedecine & Pharmacotherapy
Thematic review series: Glycerolipids. Phosphatidylserine and phosphatidylethanolamine in mammalian cells: Two metabolically related aminophospholipids
Journal of Lipid Research
Formation and function of phosphatidylserine and phosphatidylethanolamine in mammalian cells
Biochimica Et Biophysica Acta
Signaling functions of phosphatidic acid
Progress in Lipid Research
Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (Rafts)
Journal of Biological Chemistry
Identification of glycerophospholipid molecular species of mussel (Mytilus edulis) lipids by high-performance liquid chromatography-electrospray ionization-tandem mass spectrometry
Food Chemistry
Serum lipidomics profiling using LC-MS and high-energy collisional dissociation fragmentation: focus on triglyceride detection and characterization
Analytical Chemistry
Qualitative characterization of the rat liver mitochondrial lipidome using LC-MS profiling and high energy collisional dissociation (HCD) all ion fragmentation
Metabolomics
Dairy consumption and cardiometabolic health: Outcomes of a 12-month crossover trial
Nutrition & Metabolism
Cited by (29)
Nutritional value of different parts from sea eel (Astroconger myriaster) determined by untargeted-lipidomic approach
2023, Food Research InternationalBiochemical metabolomic profiling of the Crown-of-Thorns Starfish (Acanthaster): New insight into its biology for improved pest management
2023, Science of the Total EnvironmentCitation Excerpt :To a lesser degree, PS was also distinct (Supplementary Fig. S5A, B). Overall, compared to other tissues, the PC, PS and GN showed higher abundance in many lipids possibly indicating they act as lipid reservoirs, as is typical of starfish and other echinoderms as well as other marine species (Sutharshin and Sivashanth, 2011; Falch et al., 2006) (Zhang et al., 2018; Saito and Aono, 2014; Gonçalves and Lobo-da-Cunha, 2012) and other starfish (Shah et al., 2008; Díaz de Vivar et al., 2002; Lou et al., 2018). ANOVA identified 358 significantly abundant lipids between tissues (FDR: 0.05, Delta = 0.9).
The dynamic changes of flavors and UPLC-Q-Exactive-Orbitrap-MS based lipidomics in mackerel (Scomberomorus niphonius) during dry-cured processing
2023, Food Research InternationalCitation Excerpt :It is a powerful tool to identify and analyze overall components on foods due to the efficient separation capabilities of UPLC and excellent structural elucidation by HRMS (Kaufmann, 2014). Lipidomics analysis through LC-MS can be applied to identify the comprehensive lipids in meat products, and it has been applied successfully on edible shellfishes, such as Japanese abalone haliotis discushannai (Zhang et al., 2018) and marine phospholipids from different resources (Li et al., 2018). Previous studies on flavors of dry-cured mackerel are mainly focused on its volatile flavors.