Fucoid brown algae inject fucoidan carbon into the ocean

Abstract

Brown algae annually convert gigatons of carbon dioxide into carbohydrates, including the complex extracellular matrix polysaccharide fucoidan. Due to its persistence in the environment, fucoidan is potentially a pathway for marine carbon sequestration. Rates of fucoidan secretion by brown algae remain unknown due to the challenge of identifying and quantifying complex polysaccharides in seawater. We adapted the techniques of anion exchange chromatography, enzyme-linked immunosorbent assay, and biocatalytic enzyme-based assay for detection and quantification of fucoidan. We found the brown alga Fucus vesiculosus at the Baltic Sea coast of south-west Finland to secrete 0.3% of their biomass as fucoidan per day. Dissolved fucoidan concentrations in seawater adjacent to algae reached up to 0.48 mg L^-1. Fucoidan accumulated during incubations of F. vesiculosus, significantly more in light than in darkness. Maximum estimation by acid hydrolysis indicated fucoidan secretion at a rate of 28 to 40 mg C kg^-1 h^-1, accounting for 44 to 50% of all exuded dissolved organic carbon. Composed only of carbon, oxygen, hydrogen, and sulfur, fucoidan secretion does not consume nutrients enabling carbon sequestration independent of algal growth. Extrapolated over a year, the algae sequester more carbon into secreted fucoidan than their biomass. The global utility of fucoidan secretion is an alternative pathway for carbon dioxide removal by brown algae without the need to harvest or bury algal biomass.

Keywords: blue carbon; brown macroalgae; carbon sequestration; fucoidan; marine carbon cycle.

Fig. 1.

Dissolved organic carbon accumulated during brown algae incubations in the Baltic Sea in south-west Finland (A, white arrow in Left panel). Eelgrass, Zostera marina (A, Top Right panel), and bladderwrack, Fucus vesiculosus (A, Bottom Right panel), were incubated for 5 h in transparent bags with and without shading. Before and after incubations, filtered seawater oxygen (O₂), dissolved organic carbon (DOC), and total dissolved nitrogen (TDN) concentrations along with humic-like fluorescence (peak c) and chromophoric dissolved organic matter (CDOM) absorption coefficient a₍₂₅₄₎ were determined for Z. marina (B) and F. vesiculosus (C). Accumulation of mannitol and four unidentified metabolites (in arbitrary units, a.u.) in incubations could be observed using SeaMet, a derivatization and gas chromatography–mass spectrometry approach for marine samples (D and E). Asterisks indicate statistical significance (Benjamini–Hochberg adjusted P < 0.05) according to Conover–Iman test (B and C) and Wilcoxon signed rank test (D and E).

Fig. 2.

Polysaccharide-targeting techniques enabled specific quantification of dissolved fucoidan. (A) Acid hydrolyzed samples from algae incubations are plotted in a principal component analysis of monosaccharide concentrations with eigenvalue lengths of dominant monosaccharides. (B) Monosaccharide concentrations after acid hydrolysis are plotted against the summed signal absorbance at 450 nm, measured by ELISA, of two fucoidan-specific antibodies. (C) Washing with 2 M bicarbonate buffer removed considerable amounts of monosaccharides (striped bars) prior to elution with 5 M NaCl (solid bars). (D) Monosaccharide concentrations in acid hydrolyzed samples (solid bars) exceeded monosaccharides in the flow-through of AEX (striped) several folds. (E) Monosaccharides in samples, released using enzymes in the soluble cell fraction of fucoidan-metabolizing Lentimonas sp. (F) Calibration curves for monosaccharides from enzymatic digestion of fucoidan from F. vesiculosus. Abbreviations: incubation (inc.), arbitrary units (a.u.), anion exchange chromatography (AEX), fucose (Fuc), galactose (Gal), mannose/xylose (Man/Xyl), glucose (Glc), and glucuronic acid (GlcA).

Fig. 3.

Up to 50% of F. vesiculosus-secreted dissolved organic carbon was fucoidan. (A) Fucoidan obtained via AEX accounted for 13%, enzyme-confirmed fucoidan for 22% and fucoidan calculated from acid hydrolysis for 47% of secreted DOC. (B) Elemental composition of fucoidans from various brown algae shows carbon and sulfur content along with near absence of nitrogen. Abbreviations: anion exchange chromatography (AEX), Fucus (F.), Cladosiphon (C.), Durvillea (D.), Ecklonia (E.).