Unraveling the Lipidome and Antioxidant Activity of Native Bifurcaria bifurcata and Invasive Sargassum muticum Seaweeds: A Lipid Perspective on How Systemic Intrusion May Present an Opportunity

Abstract

Brown seaweeds are known to present components with appealing bioactive properties eliciting great interest for industrial applications. However, their lipid content is generally disregarded beyond their fatty acid (FA) composition. This study thoroughly characterized the lipid profile of two brown seaweeds collected from Portuguese coast, the native Bifurcaria bifurcata and the invasive Sargassum muticum species, and bioprospecting for antioxidant activity. An integrated state-of-the-art approach including gas chromatography-mass spectrometry (GC-MS) and liquid chromatography-mass spectrometry (HILIC-ESI-MS/MS), allowed a comprehensive picture of FA and polar lipid content. Polar lipid profile of B. bifurcata and S. muticum included 143 and 217 lipid species respectively, distributed between glycolipids, phospholipids, and betaine lipids. Some of the lipid species found have been assigned biological activity and contain of n-3 and n-6 FA. Sargassum muticum presented the highest n-3 FA content. Low concentrations of extracts of both seaweeds displayed antioxidant activity, with S. muticum presenting more promising results. These findings contribute to the nutritional and industrial exploitation of both seaweeds, highlighting their relevance as viable sources of bioactive and added-value compounds. Sargassum muticum presented interesting lipid composition and bioactivity, which may represent an accessible opportunity for the exploitation of this invasive seaweed, especially taking advantage of Sargassum blooms.

Keywords: antioxidant; bioactivity; lipidomics; macroalgae; mass spectrometry; nutritional quality; polyunsaturated fatty acids.

Figure 1

Relative abundance (RA) of lipid species of the sulfoquinovosyl diacylglycerol (SQDG) class identified in B. bifurcata (a) and S. muticum (b). The results are expressed as relative percentages after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA was SQDG (34:1) for both seaweeds.

Figure 2

Relative abundances (RA) of lipid species of monogalactosyl diacylglycerol (MGDG) identified in B. bifurcata (a) and S. muticum (b) and of monogalactosyl monoacylglycerol (MGMG) identified in S. muticum (c). The results are expressed as relative percentage after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA were MGDG (34:1) for B. bifurcata and MGDG (38:9) and MGMG (18:4) for S. muticum.

Figure 3

Relative abundances (RA) of lipid species of digalactosyl diacylglycerol (DGDG) glycolipids identified in B. bifurcata (a) and S. muticum (b). The results are expressed as relative percentage after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA was DGDG (38:9) for both seaweeds.

Figure 4

Relative abundance (RA) of betaine lipid species identified as diacylglyceroltrimethylhomoserine (DGTS) (a) and diacylglyceroltrimethyl-β-alanine (DGTA) (c) in B. bifurcata, and DGTS (b) and DGTA (d) in S. muticum. The results are expressed as relative percentage after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA were DGTS (34:1) and DGTA (36:4) for B. bifurcata and DGTS (34:2) and DGTA (36:4) for S. muticum.

Figure 5

Relative abundance (RA) of lipid species of the phosphatidylglycerol (PG) class identified in B. bifurcata (a) and S. muticum (b). The results are expressed as relative percentage after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA were PG (34:1) for B. bifurcata and PG (34:4) for S. muticum.

Figure 6

Relative abundance (RA) of lipid species of the phosphatidylinositol (PI) class identified in B. bifurcata (a) and S. muticum (b). The results are expressed as relative percentage after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA were PG (38:8) for B. bifurcata and PI (34:2) for S. muticum.

Figure 7

Relative abundance (RA) of lipid species of the phosphatidylcholine (PC) class identified in B. bifurcata (a) and S. muticum (b). The results are expressed as relative percentage after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA were PC (30:3) for B. bifurcata, and PC (30:3) and PC (36:4) for S. muticum.

Figure 8

Relative abundance (RA) of lipid species of the phosphatidylethanolamine (PE) class identified in B. bifurcata (a) and S. muticum (b). The results are expressed as relative percentage after dividing the normalized peak area of each lipid species to the sum of normalized peak areas for all the lipid species within the class obtained after LC–MS analysis. Numbers in parentheses (C:N) indicate the number of carbon atoms (C) and double bounds (N) in the fatty acid side chains. The species with higher RA was PC (40:8) for both seaweeds.

Figure 9

Free radical-scavenging activity (%) on 2,2´-azino-bis-3-ethylbenzothiazoline-6-sulfonic acid radical cation (ABTS) (a) and 2,2-diphenyl-1-picrylhydrazyl radical (DPPH) assays (b) radicals of B. bifurcata (a) and S. muticum lipid extracts. Each value is expressed as mean ± standard deviation (n = 3).