Article pubs.acs.org/JAFC
Lipid Profile in Different Parts of Edible Jellyfish Rhopilema esculentum Si Zhu,†,‡ Mengwei Ye,† Jilin Xu,*,† Chunyang Guo,‡ Huakun Zheng,‡ Jiabao Hu,‡ Juanjuan Chen,† Yajun Wang,‡ Shanliang Xu,‡ and Xiaojun Yan*,‡ †
Key Laboratory of Applied Marine Biotechnology of Ministry of Education and ‡Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, Ningbo University, Ningbo 315211, China S Supporting Information *
ABSTRACT: Jellyfish Rhopilema esculentum has been exploited commercially as a delicious food for a long time. Although the edible and medicinal values of R. esculentum have gained extensive attention, the effects of lipids on its nutritional value have rarely been reported. In the present of study, the lipid profile including lipid classes, fatty acyl compositions, and fatty acid (FA) positions in lipids from different parts (oral arms, umbrella, and mouth stalk) of R. esculentum was explored by ultraperformance liquid chromatography−electrospray ionization−quadrupole time-of-flight mass spectrometry (UPLC-ESI-Q-TOF-MS). More than 87 species from 10 major lipid classes including phosphatidylcholine (PC), lysophosphatidylcholine (LPC), phosphatidylethanolamine (PE), lysophosphatidylethanolamine (LPE), phosphatidylinositol (PI), lysophosphatidylinositol (LPI), phosphatidylserine (PS), ceramide (Cer), ceramide 2-aminoethylphosphonate (CAEP), and triacylglycerol (TAG) were separated and characterized. Semiquantification of individual lipid species in different parts of R. esculentum was also conducted. Results showed that glycerophospholipids (GPLs) enriched in highly unsaturated fatty acids (HUFAs) were the major compenents in all parts of R. esculentum, which accounted for 54−63% of total lipids (TLs). Considering the high level of GPLs and the FA compositions in GPLs, jellyfish R. esculentum might have great potential as a health-promoting food for humans and as a growth-promoting diet for some commercial fish and crustaceans. Meanwhile, LPC, LPE, and LPI showed high levels in oral arms when compared with umbrella and mouth stalk, which may be due to the high proportion of phospholipase A2 (PLA2) in oral arms. Moreover, a high CAEP level was detected in oral arms, which may render cell membranes with resistance to chemical hydrolysis by PLA2. The relatively low TAG content could be associated with specific functions of oral arms. KEYWORDS: jellyfish Rhopilema esculentum, lipid profile, different parts, UPLC-ESI-Q-TOF-MS
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INTRODUCTION Over the past decade, jellyfish bloom is frequently observed in marine ecosystems, which has resulted in negative effects on human activities.1,2 Although the causes, consequences, and management responses of jellyfish blooms have been explored for many years, the reduction of jellyfish numbers remains a global problem, which urgently needs to be resolved.3−5 Jellyfish is an important component of ecosystems. It was once considered as a trophic dead end in the pelagic food web, but it is now considered as an intrinsic dietary component for a large number of marine animals, such as leatherback turtle Dermochelys,6 sunfish Mola mola,7 and sliver pomfret Pampus argenteus. 8 Recently, a large number of studies have demonstrated that jellyfish has great potential as a diet supplemental diet in artificial rearing of some commercial fishes. For example, the growth of threadsail filefish juveniles can be sustained by feeding jellyfish only. In addition, fish fed both jellyfish and krill reveal a significantly faster growth than those fed krill only.9 A similar finding has been reported that phyllosomas of a scyllarid lobster can be successfully reared on jellyfish as the sole food source.10 However, the utilization of these blooming jellyfish is still limited. Thus, it is necessary to find a way to make full use of them. Rhopilema esculentum is an edible species of jellyfish that belongs to the phylum Cnidaria, class Scyphozoa, order Rhizostomeae, family Rhizostomatidae. They have been © 2015 American Chemical Society
exploited commercially as a delicious and nutrient-rich food in China for more than 1000 years and play an important role in Chinese fisheries.11 In addition, R. esculentum has been reported to have amazing functions in medicinal applications, such as lowering blood pressure and treating chronic bronchitis and a multitude of other diseases.12,13 Semidried R. esculentum can result in multimillion dollar profits in Asia.14 In addition, small-scale exploitation of jellyfish has commenced in some countries including India, Mexico, Australia, Turkey, and the United States. In recent years, R. esculentum has also been used as a diet supplement through artificial rearing of juvenile silver pomfret Pampus argenteus, an important commercial fish species with a high economic output in China. This fish species fed with R. esculentum combined with artificial diet exhibits much faster growth and higher survival rate than that fed with artificial diet alone.15 Lipids, one of the essential nutrients for organism growth and development, are considered as a source of energy and building blocks of membrane and are involved in signal transduction or hormonal regulation.16,17 Over 90% of the jellyfish body is composed of water, and other fractions are Received: Revised: Accepted: Published: 8283
June 26, 2015 August 14, 2015 August 31, 2015 August 31, 2015 DOI: 10.1021/acs.jafc.5b03145 J. Agric. Food Chem. 2015, 63, 8283−8291
Article
Journal of Agricultural and Food Chemistry mostly composed of salts, proteins, lipids, and carbohydrates.18 Despite the low content of lipids, they remain an indispensable component in jellyfish. For example, phosphonolipid (PnL), commonly present in the jellyfish, is a structural element of cell membranes and plays a special role in stabilizing cell membranes and protecting membrane lipids from hydrolytic enzymes.19 Sphingophosphonolipid (SPnL) and phospholipid (PL) from jellyfish Aurelia Aurelia and Pelagia noctiluca have been analyzed.20,21 However, no assignment of fatty acids (FAs) to the sn-1 and sn-2 positions of the glycerol backbone has been achieved. Furthermore, traditional lipid analytical methods are complex and time-consuming. For instance, the confirmation of FA compositions in each lipid class needs the separation by thin layer chromatography (TLC), fraction collection, hydrolysis by lipase, derivatization, and identification of derivatized FAs by gas chromatography (GC) or gas chromatography coupled with mass spectrometry (GC-MS). Nuclear magnetic resonance (NMR) and electrospray ionization mass spectroscopy (ESIMS) have been also used to characterize glycolipids and SPnL in Phyllorhiza punctata.22 Even though detailed structural information on monogalactosyldiacylglycerol (MGDG), sulfoquinovosyldiacylglycerol (SQDG), and ceramide 2-aminoethylphosphonate (CAEP) has been obtained, a series of complex steps are still required to separate lipids by TLC. In addition, the infusion of crude lipid extracts into ESI-MS could result in a significant loss of ion signals from those lowabundance components.23 Fortunately, this problem can be avoided by the separation of crude lipids using chromatography. Recently, the comprehensive characterization of a variety of lipids in marine organisms has been achieved by using UPLC coupled with Q-TOF MS in a MSE data collection mode24,25 without the requirement of preseparation. In the present study, the comprehensive characterization and semiquantification of lipid profile in different parts of jellyfish R. esculentum were conducted by ultraperformance liquid chromatography−electrospray ionization−quadrupole time-of-flight mass spectrometry (UPLC-ESI-Q-TOF-MS), which will facilitate the evaluation of the nutritional value of R. esculentum as a healthy food for humans or as a diet supplement for commercial fish.
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acetonitrile/isopropanol/tetrahydrofuran (1:1:1, v/v/v) and mobile phase B composed of water/acetonitrile (1:2, v/v), both containing 0.1% formic acid as well as 0.01% lithium acetate. Efficient separation of lipids was achieved with a gradient elution: 0−3 min, 2% A; 3.0−5.0 min, 2−30% A; 5−12 min, 30−50% A; 12−22 min, 50−80% A; 22−25 min, 80% A; 25−27 min, returning to initial 2% A; 27−30 min, 2% A. The temperature of the sample chamber was set at 6 °C, the column temperature was set at 40 °C, and the injection volume was 3 μL for each analysis. Before injection, samples were filtered with a 0.22 μm ultrafiltration membrane (Millipore, Bedford, MA, USA). Mass Spectrometric Analysis. Mass spectrometric analysis was performed on a Waters Q-TOF Premier mass spectrometer in both positive and negative ion modes. The mass range was from 150 to 1200 with a scanning duration of 0.3 s. The nebulization gas was set at a constant flow rate of 600 L/h at 400 °C, and the source temperature was set at 120 °C. Compositions and contents of TLs were detected in both positive and negative modes. For positive mode, the capillary voltage was set at 3.0 kV; the sampling cone voltage was set at a ramp of 25−40 V, whereas for negative mode, the capillary voltage was set at 2.6 kV and the sampling cone voltage was set at a ramp of 25−40 V. MSE analysis was performed on the mass spectrometer with the setting at 6 kV for low collision energy and a ramp of 25−50 kV for high collision energy. The time-of-flight analyzer was used in V mode and tuned for maximum resolution (>10000 resolving power at m/z 1000). The instrument was previously calibrated with sodium formate, and the lock mass spray for precise mass determination was set by leucine enkephalin ([M + H]+ at m/z 556.2771 and [M − H]− at m/z 554.2615) at a concentration 0.2 ng/mL, which makes the maximum relative error up to 5 ppm. Identification of Lipids by ESI-MS. The exact masses (the mass difference was
