Lipidomics and Anti-Inflammation Activity of Brown Algae, <i>Lobophora</i> sp., in Vietnam

Pham, Thu Hue; Nguyen, Van Tuyen Anh; Do, Thi Thanh Trung; Do, Anh Duy; Dam, Duc Tien; Tran, Thi Thanh Van; Pham, Quoc Long; Le, Tat Thanh

doi:https://doi.org/10.1155/2020/8829054

Journal of Chemistry

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Abstract Introduction Materials and Methods Results and Discussion Discussion Conclusions Data Availability Conflicts of Interest Acknowledgments Supplementary Materials References Copyright Related Articles

Research Article | Open Access

Volume 2020 | Article ID 8829054 | https://doi.org/10.1155/2020/8829054

Lipidomics and Anti-Inflammation Activity of Brown Algae, Lobophora sp., in Vietnam

Thu Hue Pham,^1,2Van Tuyen Anh Nguyen,³Thi Thanh Trung Do,³Anh Duy Do,⁴Duc Tien Dam,⁵Thi Thanh Van Tran,⁶Quoc Long Pham,³and Tat Thanh Le^1,3

Academic Editor: Andrea Mastinu

Received02 Oct 2020

Revised23 Nov 2020

Accepted27 Nov 2020

Published09 Dec 2020

Abstract

Lobophora sp., belonging to brown macro algae phylum, is found in coral reefs. In this study, the fatty acid composition, lipid classes, polar lipid molecular forms, and bioactivities of this algae have been determined. It follows that five classes including polar lipid (Pol), sterol (ST), free fatty acids (FFA), triacylglycerol (TAG), and hydrocarbon and wax (HW), 23 fatty acids containing 5 PUFAs (ALA, GLA, AA, EPA, and DHA) and 157 molecular types of polar lipid group containing 48 phospholipid molecular forms belonging to 4 subclasses (PI (11), PC (14), PG (22), PA (1)), 45 glycolipid molecular forms classified into 3 subclasses of MGDG (8), DGDG (1), SQDG (36), and 64 betaine lipid molecular forms belonging to 2 subclasses (DGTA (37), DGTS (27)) have been identified for the first time from this algae. Furthermore, both polar lipid (PL) and unpolar lipid (UPL) show the NO inhibition activities with values of IC₅₀ ranging from 52.10 to 66.21 µg/mL. Thus, lipid of this brown algae could promise to be a potential source for application in food, cosmetic, and pharmaceutic industry.

1. Introduction

Plants produce secondary metabolites as signals to interact with the environment and stresses [1, 2]. A number of secondary metabolites from seaweeds have been detected to have such valuable bioactivities as antibacterial, anti-viral, anti-cancer, and antioxidant. In Vietnam, the brown seaweed genus Lobophora belongs to the family Dictyotaceae, found worldwide in tropical to temperate waters and discovered in the coral reef. From the early 1980s to 2017, 49 scientific works have been reported on chemicals and bioactivities of Lobophora genus, in which 40 have been reported with bioactivities. Particularly, most of the studies have been centered on Lobophora variegata, while other species have been still poorly studied and reported [3]. Until now, there have been few studies on lipidomic profile and their bioactivities.

Certain lipid classes have been identified in several algae including polar (Pol), sterol (ST), diacylglycerol (DG), free fatty acids (FFA), triacylglycerol (TG), monoalkyldiacylglycerol (MADG), and hydrocarbons and wax (HW) [4], while neutral lipid classes play various roles such as storing energy or pre-hormones for the body; the polar lipid class has been especially considered for its various bioactivities such as acting as antioxidant and helping in curing cardiovascular diseases and cancer caused by long chain polyunsaturated fatty acids (PUFAs) [5, 6]. Some high level PUFAs containing C20 fatty acids such as 20:4n-6 (AA), 20:5n-3 (EPA), and 20:3n-6 have been identified and evaluated bioactivities in 7 brown seaweed species belonging to the genera Sargassum, Cystoseira, Padina, and Turbinaria. Other PUFAs have been identified as 22:6n-3 (DHA), which is a highly valuable bioactive fatty acid for application in medicine and food [7]. In addition to being sources of PUFA, the polar lipids have an important role in structural function as components of cell membranes [8].

In algae, fatty acids are found in the esterified structure such as glycoglycerolipids (GLs), glycerophospholipids (PLs), and betaine lipids [9]. The research on the lipidomics is essential to identify new bioactive compounds and properties based on the polar lipid composition [10]. Moreover, it is also a critical step to the discovery of fostering bio-prospection of lipidic extracts.

Nowadays, mass spectrometry (MS) coupled with liquid chromatography (LC) technique is usually used to determine the detailed structural characterization of lipids and to fully explore lipidomic signature of distinct matrices [11, 12] and identify lipidome signature of cultivated seaweeds Ulva lactuca Linnaeus [13], Chondrus crispus Stackhouse [14], and Codium tomentosum Stackhouse [15]. However, there has been no report on Lobophora genus lipidome.

This study aims to analyse and identify the lipid characterisation of species Lobophora sp. first collected at Con Dao, Ba Ria-Vung Tau, Vietnam, by using high-performance liquid chromatography in combination with high-resolution mass spectrometry (HPLC-HRMS). The lipid extracts have also been pre-tested for anti-inflammatory effects by inhibiting the production of NO.

2. Materials and Methods

The Lobophora sp. samples were collected in Con Dao, Ba Ria-Vung Tau, Vietnam. Chemicals were obtained from Sigma, Merck, that reached the purification standards for analysis and HPLC grade.

2.1. Total Lipid Extraction

Total lipid was extracted according to method of Bligh and Dyer [16] and Nguyen et al. [17]. Polar lipids were obtained by the silica column. The 200 mg of total lipid was dissolved in chloroform and loaded on the silica column (Phillipsburg, NJ), washed by 44 ml chloroform to remove the pigments and neutral lipid, and then eluted by 120 ml MeOH 95% to obtain polar lipids. The obtained fractions were stored in chloroform at –5°C for analysis.

2.2. Analyses of Lipid Classes

Total lipids were dissolved in CHCl₃ (10 mg/ml) and spotted on the Sorbfil thin plate (6 × 6 cm). The n-hexane/diethyl ether/acetic acid (85/15/1, v/v/v) solvent was applied to identify neutral lipid layers; then, the CHCl₃/CH₃OH (2/1, v/v) solvent was applied to identify the polar lipid layer. The TLC was displayed by 10% H₂SO₄/CH₃OH reagent at 240^°C for 10 minutes. The image of thin layer was obtained using Epson Perfection 2400 scanner, Japan, with grayscale mode. The lipid layers on the thin plate and the percentage of the layers were identified by light sensitivity on the Sorbfil TLC Analysis software Video densitometer, Krasnodar, Russia [17, 18].

2.3. Analyses of Fatty Acids

Fatty acid methyl esters (FAMEs) were obtained by incubating total lipid with 2% H₂SO₄ in CH₃OH at 80°C for 2 hrs and then cleaned by TLC in the hexane:diethyl ether, 95/5 (v/v) solvent. FAMEs were analysed on Shimadzu GC-2010 gas chromatograph (Kyoto, Japan) using flame ionization detector (FID) on Capillary Equity 5 (Merck, L × ID 30 m × 0.25 mm, df 0.25 µm). Carrier gas was He at the speed of 20 ml/min. Temperature program in the oven operating was at 160°C, raised 2°C/min to 240°C, and then kept for 20 minutes. Fatty acids were identified by the equivalent retention time value, Equivalent Chain Length, with the standard system of fatty acids C16 : 0 and C18 : 0. The fatty acid structures were identified by GC-MS. The spectra were compared with the NIST library and fatty acid mass spectra archive [17, 18].

2.4. Analysis of Molecular Species of Polar Lipids

The molecules of polar lipids were analysed by high-performance liquid chromatography combined high resolution mass spectrometry (HPLC-HRMS) with Shim-Pack diol column (ID 50 mm × 4.6 mm, carrier size 5 μm, Shimadzu, Kyoto, Japan). The polar lipid classes were separated by HPLC in a solvent A: n-hexane/2-propanol/formic acid/(C₂H₅)₃N and the solvent B: 2-propanol/H₂O/formic acid/(C₂H₅)₃N [19] and then detected by the high-resolution ion trap over time of mass spectrometry using the LC/MS-IT-TOF (Shimadzu) device, an electronic atomizing ionization source (ESI) device. Flow rate was 0.2 ml/min [17, 20, 21].

2.5. Nitric Oxide Production Inhibition Assay

In vitro anti-inflammatory activity of lipid samples was elucidated by using nitric oxide (NO) assay as described previously by Mosmann [22] using the Griess reagents (Promega, USA). The RAW 264.7 cells at the concentration of 2 × 10⁵ cells/mL were dropped on the 96-well plate and incubated in 37^°C with 5% CO₂ in 24 h. The culture medium was exchanged to Dulbecco’s Modified Eagle’s Medium (DMEM) (Life Technologies, USA) with no fetal bovine serum (FBS) for 3 hours. The cells were incubated with the lipid fractions at different concentrations before stimulating the NO production by LPS (1 µg/mL) for 24 hours. Then, the amount of nitrite in the culture medium was measured by Griess reaction at room temperature for 10 minutes. The fresh culture medium was used as a blank, while L-NMMA (Sigma) was tested as the positive sample. The mixtures were quantified spectrophotometrically at 540 nm using a micro-plate reader (ELx800 Biotekm, USA). The sodium nitrite was used as a standard compound to establish the standard curve. The NO inhibition was calculated following the formula: %NO inhibition = 100% − [concentration of NO_sample/concentration of NO_LPS]100. IC50s were calculated by TableCurve 2Dv4 software.

The cell viability test was performed parallel with the NO inhibition assay. The 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) was used to evaluate cell viability because active cells transform the water-soluble MTT to an insoluble purple formazan. 20 μl lipid sample and 180 µL of RAW 264.7 cells were put into 96-well plates and then incubated with 5% CO₂ for 72 hours at 37°C. After adding MTT (5 µg/mL), the mixtures were incubated for 4 hours and supernatant was removed. The formazan crystals were dissolved in DMSO and measured at 540 nm. The percentage of cell viability was determined by comparing to the control samples.

3. Results and Discussion

3.1. Total Lipid

Total lipid content from brown algae Lobophora sp. is 1.06 ± 0.2% weight of fresh algae, similar to the brown samples previously studied [4, 23]. Compositions and contents of total lipid classes of Lobophora sp. are shown in Figure 1 and Table 1. Pol class accounts for the highest level of 26.8% compared with the detected classes, following by 4 classes of TG, FFA, ST, and HW with the content of 26.0%, 25.9%, 18.5%, and 2.7%, respectively.

3.2. Fatty Acids Composition

In the lipid composition of Lobophora sp. (Table 2), 23 fatty acids C12–C22 are identified. SAFAs contain 8 fatty acids 12 : 0, 14 : 0, 15 : 0, 16 : 0, 17 : 0, 18 : 0, 20 : 0, and 22 : 0, in which 14 : 0 (9.62%) and 16 : 0 (12.04%) have high contents. MUFAs group has 16 : 1n-5, 16 : 1n-7, 18 : 1n-7, and 18 : 1n-9, in which 18 : 1n-9 (11.53%) is typical. PUFAs group has 11 fatty acids including 18 : 2n-6, 18 : 3n-3, 18 : 3n-6, 18 : 4n-3, 20 : 2n-6, 20 : 3n-6, 20 : 3n-9, 20 : 4n-3, 20 : 4n-6 (AA) 20 : 5n-3 (EPA), and 22 : 6n-3 (DHA), in which AA (12.14%), EPA (11.56%), and DHA (14.26%) are significant.

3.3. Molecular Species of Polar Lipids

Three subclasses including phospholipid, glycolipid, and betaine lipid were identified in 26.80% polar lipid (Pol).

First, the phospholipid subclass contains 4 groups of phosphatidylinositol (PI), phosphatidylcholine (PC), phosphatidylglycerol (PG), and phosphatidic acid (PA). In PI group, 13 molecular forms were found, of which 11 forms had complete formula with one PI isomer form and no alkenyl acyl glycerophosphoinositol (Table 3).

In particular, PI 34 : 1 is recognized at the highest rate of 44.09% PI Figure (1S). On the MS⁻ spectrum, the ion [M − H]⁻ has the strongest signal at m/z 835.5283 corresponding to ion [C₄₃H₇₉O₁₃P]⁻ (calculated 836.5415, different 0.00620). The MS²⁻ spectrum shows signals at m/z 255.2338 corresponding to the anion of 16 : 0 fatty acids and m/z 281.2471 to the anion of 18 : 1 fatty acid. Importantly, fragment at m/z 297.0334 is the considered ion [C₄₃H₇₉O₁₃P]⁻ that lost the diacyl group which is the characteristic fragmentation to determine the PI molecular forms. Thus, the mass spectrometry data prove that the considered molecule is diacyl glycerophosphoinositol PI 16 : 0/18 : 1 or PI 34 : 1.

In the PC group, 18 molecular forms have been identified, in which 14 molecular forms are completely identified with one isomer (Table 3). The PC fragmentation has been observed on both MS⁻ and MS⁺ with signals of ions [M + H]⁺, [M + HCOO]⁻, and [M − CH₃]⁻. For example, the PC 30 : 0 with highest content of 19.3% is recognized with the appearance of [M + H]⁺ signal at m/z 706.5375 corresponding to [C₃₈H₇₇NO₈P]⁺ (calculated 705.5309, different 0.00063) and two signals at m/z 750.5226 and m/z 690.5025 corresponding to ion [M + HCOO]⁻ and ion [M − CH₃]⁻, respectively (Figure 2S). On the MS²⁻spectrum, the signal at m/z 690.5088 is formed by removing a C₂H₄O₂ molecule (methyl formate) from the ion at m/z 750.5226. Besides, two fragments at m/z 227.2042 corresponding to ion of 14 : 0 fatty acid (calculated 228.2089, different 0.00255) and at m/z 255.2262 to ion of 16 : 0 fatty acid (calculated 256.2402, different 0.00675) have resulted. Therefore, PC 30 : 0 has been identified as diacyl glycerophosphocholine, PC 14 : 0/16 : 0.

In the PG group, 15 molecular forms have been determined with complete formula, in which 6 PGs are detected with isomers (Table 3). PG 34 : 2 is found at the highest rate of 41.83%. On the MS⁻, signal of ion [M − H]⁻ is observed with the strongest intensity at m/z 745.4985 corresponding to ion [C₄₀H₇₄O₁₀P]⁻. The MS²⁻ of the ion [C₄₀H₇₄O₁₀P]⁻ (Figure 3S) contains a signal at m/z 253.2137 (calculated 254.2246, different 0.0009) corresponding to 16 : 1 fatty acid and signal at m/z 281.2485 (calculated 282.2559, different 0.0026) corresponding to 18 : 1 fatty acid. Besides, there have been 3 signals including at m/z 417.2395; 491.2738; 509.2838 corresponding to molecules which have lost glycerol and acyl groups of 16 : 1 fatty acid anion; a 16 : 1 fatty acid; a ketene group of 16 : 1 fatty acid anion, respectively. In addition, the MS²⁻ (Figure 3S) shows a lower intensity signal at m/z 279.2349 (calculated 280.2402, different 0.00195) corresponding to the carboxylate anion of 18 : 2 fatty acid. This indicates that there is an isomer of PG 34 : 2 with composition containing 18 : 2 and 16 : 0 fatty acids. The above data demonstrate that the molecular ion value m/z 745.4985 presents two isomers including PG 16 : 0/18 : 2 and PG 16 : 1/18 : 1, in which PG 16 : 1/18 : 1 is the major content.

With the PA molecular forms, only one PA 40 : 8 is identified (Table 3). On the MS⁻ spectrum of PA, ion [M-H]⁻ is observed with the strongest signal at m/z 743.4609 (calculated 744.4730, different 0.00483, 11 double bonds) corresponding to ion [C₄₃H₆₈O₈P]⁻ (Figure 4S). On the MS²⁻, fragments have been found with the signals at m/z 457.2260 and m/z 439.2215 corresponding to the considered PA fragment which has lost a dehydrated molecule of 20 : 4 and a 20 : 4 fatty acids, respectively. Additionally, the signal at m/z 303.2243 is the acyl carboxylate ion of 20 : 4 fatty acid. With the above data, PA 40 : 8 is identified as diacyl glycerophosphatic acid PA 20 : 4/20 : 4.

Second, in the glycolipid subclass, 3 groups have been identified including monogalactosyldiacylglycerol (MGDG), digalactosyldiacylglycerol (DGDG), and sulfoquinovosyldiacylglycerol (SQDG). In the MGDG group, 21 molecular forms are identified, in which 8 have been completely identified (Table 4).

For example, with the highest ratio of 13.92%, MGDG 38 : 9 has formed molecular ions (Figure 5S). On the MS⁻, the ion [M + HCOO]⁻ signal at m/z 841.5021 corresponds to ion [C₄₈H₇₃O₁₂]⁻ and the ion [M − H]⁻ signal at m/z 795.5046 corresponds to ion [C₄₇H₇₁O₁₀]⁻. On the MS⁺, the ion [M + Na]⁺ has the strongest signal at m/z 819.5023 corresponding to [C₄₇H₇₂O₁₀Na]⁺. On the MS²⁺ of [C₄₇H₇₂O₁₀Na]⁺ ion, it has been simultaneously observed with two signals at m/z 543.2932 and 517.2795 corresponding to the considered MGDG molecule lost fragments of m/z 276.2091 [C₁₈H₂₇O₂]⁻ (18 : 4 fatty acid) and m/z 302.2228 [C₂₀H₂₉O₂]⁻ (20 : 5 fatty acid), respectively. The obtained data show that the MGDG 38 : 9 is 18 : 4/20 : 5.

In the DGDG group, only one DGDG form has been found as DGDG 34 : 1 which is described in Table 4 and Figure 6S. On the MS⁺ spectrum, the ion [M + Na]⁺ has the signal at m/z 941.6144 corresponding to ion [C₄₉H₉₀O₁₅Na]⁺. On the MS⁻ spectrum, the ion [M − H]⁻ has the strongest signal at m/z 917.6080 corresponding to ion [C₄₉H₈₉O₁₅]⁻ (calculated 917.6116, different 0.00580). On the MS²⁻ spectrum of ion [C₄₉H₈₉O₁₅]⁻, there have been simultaneously signals at m/z 661.3696 and m/z 635.3551 corresponding to the considered DGDG molecule that has lost neutral fragments including 16 : 0 fatty acid (m/z 256.2420) and 18 : 1 fatty acid (m/z 282.2565). The above data indicate that the molecular form is DGDG 16 : 0/18 : 1.

In the SQDG group, 26 complete molecular forms have been identified with 10 isomers (Table 4). A molecule with the highest content of 21.78% is identified as SQDG 34 : 1. On the MS⁻ spectrum, the ion [M − H]⁻ of SQDG 34 : 1 is observed with the strongest signal at m/z 819.5162 corresponding to ion [C₄₃H₇₉O₁₂S]⁻ (Figure 7S). On the MS²⁻ spectrum, the signal at m/z 581.2991 is formed when the ion at m/z 819.5162 eliminates a dehydrated molecule of fatty acid 16 : 0. The signal at m/z 563.2831 has also been observed in the MS²⁻ spectrum simultaneously. This signal appears when the ion [C₄₃H₇₉O₁₂S]⁻ loses fatty acid 16 : 0. In addition, the appearance of signal m/z 281.2489 (calculated 282.2559, different 0.00030) corresponds to anion of 18 : 1 fatty acid. Thus, data show that the obtained SQDG 34 : 1 is 16 : 0/18 : 1.

In addition to phospholipid and glycolipid classes, betaine lipid subclass includes 2 groups of DGTA and DGTS. In the DGTA group, 37 molecular forms have been identified, in which 29 forms are completely identified with 8 isomers (Table 5). Among those, DGTA 34 : 1 is the highest content of 10.20%. On the MS⁺ spectrum, the ion [M + H]⁺ has the strongest signal at m/z 738.6298 corresponding to ion [C₄₄H₈₄NO₇]⁺. On the MS²⁺ spectrum, there have been simultaneously two signals at m/z 500.3955 and 482.3784 corresponding to the ion [C₄₄H₈₄NO₇]⁺ that has lost a dehydrated molecule of fatty acid 16 : 0 and a neutral fragment of 16 : 0 fatty acid. Besides, the ion [C₄₄H₈₄NO₇]⁺ has lost a dehydrated molecule of 18 : 1 fatty acid and formed a signal at m/z 474.3783. This ion eliminates water molecule and shows signal at m/z 456.3806. In addition, the signal at m/z 236.1485 is semimolecule ion of DGTA that lost diacyl groups, which is a very important signal in determining the molecular forms of DGTA (Figure 8S). Thus, the above data prove that the considered molecule is DGTA 16 : 0/18 : 1.

There are 23 molecular forms with 13 isomers identified in DGTS subclass (Table 5). The DGTS molecular form at the highest ratio of 19.21% is DGTS 28 : 0. On the MS⁺ spectrum, the ion [M + H]⁺ has the strongest signal at m/z 656.5459 corresponding to ion [C₃₈H₇₄NO₇]⁺ (Figure 9S). On the MS²⁺ spectrum, signal at m/z 446.3490 appears because the ion [C₃₈H₇₄NO₇]⁺ loses a dehydrated molecule of acid 14 : 0. Signal at m/z 428.3395 has also been observed in the MS²⁺ spectrum. This signal corresponds to the ion [C₃₈H₇₄NO₇]⁺ that loses a neutral fragment of 14 : 0 fatty acid. In addition, the appearance of signal at m/z 236.1517 is important for detection of the molecular form of DGTS. It is similar to the determination of DGTA. Thus, the above data prove that the considered molecule is DGTS 14 : 0/14 : 0.

3.4. Anti-Inflammatory Activity

Three lipid fractions yield the inhibitory effects on NO production in RAW 264.7 cells. The IC₅₀ values have been evaluated from 52.10 to 66.21 µg/mL (Table 6). The unpolar lipid fraction (UPol) has a strongest activity IC₅₀ of 52.10 ± 4.43, following by total lipid and polar lipid samples with IC₅₀ of 61.09 ± 6.06 and 66.21 ± 6.24 µg/mL, respectively. All fractions do not exhibit the cytotoxicity with the cell viability from 96.06 to 100% at the concentration of 100 µg/mL, while the control sample shows the cell viability percentage of 89.90% with the same concentration (Table 6).

4. Discussion

In the total lipid of Lobophora sp., 5 classes including Pol, ST, FFA, TG, and HW have been found, while other brown algae samples from the genus Sargassum collected in Vietnam show three or four classes of Pol, ST, FFA, and TG [4, 23]. In contrast to terrestrial plants with high content of 16C and 18C fatty acids, Lobophora sp. has low content of 16C and 18C fatty acids similar to brown seaweeds reported [4]. Particularly, lipid composition of Lobophora sp. contains a variety of fatty acids (23 types) including many long chains and 6 double bonds fatty acids belonging to ω3 (n-3) and ω6 (n-6) with 23.40% and 34.15% of the total FA, respectively. They have been considered to be beneficial for the human brain and overall health, including cardiovascular effects, improving the function of the heart and the liver, reducing blood pressure, anti-thrombosis, and helping with arthritis, cancer, and lung diseases [24–28]. Among those, α- and γ-linolenic acids (C18 : 3n-3-ALA and C18 : 3n-6-GLA) have the total content of 11.93%, which are very important fatty acids in the formation and protection of the skin to potentially apply in the cosmetic industry [29].

Previous research has shown that the fatty acid composition in seaweed contains saturated fatty acids (SFAs) with high content and polyunsaturated fatty acids (MUFAs, PUFAs) with very low content. For example, the green algae Ulva rigida has 64.5% SFAs, 23.78% PUFAs, and 11.71% MUFAs [9]. The brown algae Padina pavonica has those with content of 43.45%, 1.7%, and 23.67%, respectively [30]; some red algae species belonging to Hypnea genus in Vietnam had the content of SFAs >60%, PUFAs from 3–12%, and MUFAs is 8.55–27.88% [31]; other red algae have the similar fatty acid profile [32, 33]. Interestingly, the fatty acid profile of this Lobophora sp. revealed the high level of polyunsaturated fatty acids (MUFAs, PUFAs) with the content of 75.10%, which is extremely noteworthy to further study for potential application.

Lobophora sp. is an infrequent species that has been detected with 6 PUFAs belonging to the C20 fatty acid group including C20 : 2n-6; C20 : 3n-6 (DGLA); C20 : 3n-9; C20 : 4n-3; C20 : 4n-6 (AA); C20 : 5n-3 (EPA), in which DGLA, AA and EPA have content of 1.12%, 12.14%, and 11.56%, respectively. They are precursors which provide the initial fatty acids for the biosynthesis process of eicosanoids. Those are signaling molecules that control many systems in the human body, of which the most important roles are involved in the inflammatory process, immune response, and the effect on the central nervous system [33–35].

Particularly, the fatty acid C22 : 6n-3 (DHA) has been identified in the total lipid of this species with the content of 14.26% which is a valuable fatty acid in foods that helps increase the brain development of children and young animals [36]. DHA content of this species is much higher than that of other brown seaweeds collected in Vietnam and of oysters, fish, and corals [4, 18, 35]. This can be a sign to distinguish seaweeds living in coral reefs from those living in coastal areas.

Recent researches on lipid usually have applied GC-MS, GC-FID techniques to detect the composition and content of fatty acids; however, fatty acids exist in both free and linked types. Nowadays, the application of HR-MS technique helps identify the hold of lipid molecules and even molecular species based on ion values of MS [17, 18, 21]. Some novel techniques such as LC-MS/MS have been applied to study the lipidome of seaweed [9, 10, 14, 15, 37]. With HPLC-HRMS technique, 157 polar lipids molecular forms have been, for the first time, identified belonging to phospholipids, glycolipids, and betaine lipids of Lobophora sp.

Betaine lipids are an amphoteric subclass like phospholipids because they have a positively charged ammonium group. They are determined to have a function similar to phospholipids in many algae, fungi, and seedless plants [38–42]. DGTA is a glycerol-lipid that contains two fatty acids esterified with glycerol and an ether-linked polar group derived from an amino acid, while DGTS is an isomer structure and biosynthetic precursor of DGTA in the algae [43, 44]. The coexistence of DGTS and DTGA in many types of algae can be explained by a partial conversion of DGTS to DGTA.

In addition to molecular species analysis, the total lipid from Lobophora sp. has been separated into polar lipid and unpolar lipid fractions, in which polar lipid contained phospholipid, betaine lipid, and glycolipid classes. In recent studies, the extracts from Lobophora species have been reported on such bioactivities as anti-oxidant, anti-inflammation, anti-microbial, and cytotoxic activities [3]. In this study, we have preliminarily screened the anti-inflammation activity of three lipid fractions through the NO production inhibition assay because NO is a key signaling molecule in the inflammation process [45]. The results show that the lipid fractions exhibited the strong NO production inhibition activity.

Particularly, the unpolar lipid fraction displays a higher NO inhibitory activity than polar lipid. This result contrasts with what has been reported on lipid fraction from a mud crab Scylla paramamosain, which shows the inhibition of the polar lipid higher than the unpolar lipid fraction [19]. This may be caused by the polar lipid content of Lobophora sp. which is lower than that of the mud crab S. paramamosain, 26.8% and 40.02%, respectively. Other authors have demonstrated that an abundance of PUFAs in seaweed composition related to the display of anti-inflammatory activity [9, 46]. It has also been reported that anti-inflammatory activities (IC₅₀) of seafood range from 64.6 to 306.4 µg/mL. In this report, the NO inhibition activity of lipid fractions is comparable to those of Octopus lipids [47] and sulfated polysaccharide of the marine brown algae Lobophora variegata [48]. Particularly, it is the first time that the Lobophora sp. lipid fractions have been demonstrated strong NO inhibition activity.

The recent reports indicate that the production of NO is increased by neuronal nitric oxide synthase (nNOS) mediated by the NF-κB factor [49]. In addition, the transcription of Nf-κB has been regulated by n-3 PUFAs [50]. Also, the report of Echeverria shows that n-3 PUFAs (especially EPA and DHA) partially reduce the proinflammatory indexes such as NF-κB and Nrf2 [51]. Thus, it suggests that lipid fractions containing n-3 PUFAs may inhibit NO inhibition through regulation of factors NF-κB and Nrf2.

In several expert studies, total extracts, their fractions, and molecular species have demonstrated bioactivities [52–56]. Particularly, glycolipids from different algae species have anti-viral, antibacterial, and anti-tumoral activity [53, 54]. SQDG (32 : 0) and SQMG (16 : 0) are both described to have anti-microbial activity [55, 56]. Some reports suggest that DGTS has the same function as PC due to their similar zwitterionic structure, and they are interchangeable in the cell [44]. It is significant that the MGDG displays anti-inflammatory activity and is combined with omega-3 to treat the regeneration of articular cartilage in the osteoarthritis adult. Thus, further study will be focusing on evaluating the bioactivities of the composition of Lobophora sp. lipid such as fatty acids, lipid classes, and molecular species.

5. Conclusions

In summary, lipid classes and fatty acid profile of seaweed Lobophora sp. have been well defined. The simultaneous detection of high-value long-chain polyunsaturated fatty acids such as AA, EPA, and DHA in this seaweed has inspired researches to study the origin of these fatty acids in the reef ecosystem. HPLC-HRMS technique has allowed identifying 157 molecular forms in polar lipid that are classified into betaine lipid, glycolipid, and phospholipid groups with 64, 45, and 48 molecular forms, respectively. The NO inhibition effects of lipid fractions including total lipid, polar lipid, and unpolar lipid have been reported for the first time with IC₅₀ from 52.10 to 66.21 µg/mL. These all suggest that Lobophora sp. lipids need to be further studied for potential application in food, medicine, and cosmetics.

Data Availability

No data were used to support this study.

Conflicts of Interest

The authors declare no conflicts of interest.

Acknowledgments

The authors would like to express their sincere thanks to the Laboratory of Comparative Biochemistry A. V. Zhirmunsky Institute of Marine Biology, Far-Eastern Branch of the Russian Academy of Sciences, 17 Palchevskogo str., Vladivostok 690041, Russian Federation. Furthermore, the authors are grateful to the Project “Researching and Assessing the Potential of Resources and the Ability to Exploit and Cultivate Seaweed in Economic Target Islands in Service of Socio-Economic Development” (Code: KC.09.05/16-20) for supporting their study.

Supplementary Materials

Figure 1S. HPLC-HRMS and fragmentations of PI 34 : 1 [C₄₃H₇₉O₁₃P]⁻. (a) HPLC-HRMS chromatogram of [C₄₃H₇₉O₁₃P]⁻. (b) Negative mass spectrometry (MS⁻) of [C₄₃H₇₉O₁₃P]⁻. (c) Negative mass spectrometry (MS²⁻) of signal at m/z 835.5283. Figure 2S. HPLC-HRMS and fragmentations of PC 30 : 0 [C₃₈H₇₇ NO₈P]⁺. (a) HPLC-HRMS chromatogram of [C₃₈H₇₇ NO₈P]⁺. (b) Positive mass spectrometry (MS⁺) of signal at m/z [C₃₈H₇₇ NO₈P]⁺. (c) Negative mass spectrometry (MS⁻) of signal at m/z 690.5025 and m/z 750.5026. (c) Negative mass spectrometry (MS²⁻) of signal at m/z 690.5025. Figure 3S. HPLC-HRMS and fragmentations of PG 34 : 2 [C₄₀H₇₄O₁₀P]^-. (a) HPLC-HRMS chromatogram of [C40H74O10P]⁻. (b) Negative mass spectrometry (MS⁻) of [C40H74O10P]⁻. (c) Negative mass spectrometry (MS²⁻) of signal at m/z 745.4985. Figure 4S. HPLC-HRMS and fragmentations of PA 40 : 8 [C₄₃H₆₈O₈P]⁻. (a) HPLC-HRMS chromatogram of [C43H68O8P]⁻. (b) Negative mass spectrometry (MS⁻) of [C43H68O8P]⁻. (c) Negative mass spectrometry (MS²⁻) of signal at m/z 743.4609. Figure 5S. HPLC-HRMS and fragmentations of MGDG 38 : 9 [C₄₇H₇₂O₁₀Na]⁺. (a) HPLC-HRMS chromatogram of [C47H72O10Na]⁺. (b) Positive mass spectrometry (MS⁺) of [C47H72O10Na]⁺. (c) Negative mass spectrometry (MS⁻) of signal at m/z 795.5046 and m/z 841.5021. (d) Positive mass spectrometry (MS²⁺) of signal at m/z 819.5023. Figure 6S. HPLC-HRMS and fragmentations of DGDG 34 : 1 [C₄₉H₈₉O₁₅]⁻. (a) HPLC-HRMS chromatogram of [C49H89O15]⁻. (b) Negative mass spectrometry (MS⁻) of [C49H89O15]⁻. (c) Negative mass spectrometry (MS⁻) of [C49H89O15Na]⁺. (d) Negative mass spectrometry (MS²⁻) of m/z 917.600. Figure 7S. HPLC-HRMS and fragmentations of SQDG 34 : 1 [C₄₃H₇₉O₁₂S]⁻. (a) HPLC-HRMS chromatogram of [C43H79O12S]⁻. (b) Negative mass spectrometry (MS⁻) of [C43H79O12S]⁻. (c) Negative mass spectrometry (MS²⁻) of signal at m/z 819.5162. Figure 8S. HPLC-HRMS and fragmentations of DGTA 34 : 1 [C₄₄H₈₄NO₇]⁺. (a) HPLC-HRMS chromatogram of [C44H84NO7]⁺. (b) Positive mass spectrometry (MS⁺) of [C44H84NO7]⁺. (c) Positive mass spectrometry (MS²⁺) of signal at m/z 738.6298. Figure 9S. HPLC-HRMS and fragmentations of DGTS 28 : 0 [C₃₈H₇₄NO₇]⁺. (a) HPLC-HRMS chromatogram of [C38H74NO7]⁺. (b) Positive mass spectrometry (MS⁺) of [C38H74NO7]⁺. (c) Positive mass spectrometry (MS²⁺) of signal at m/z 656.5459. . (Supplementary Materials)

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