Laminarin is a major molecule in the marine carbon cycle

Abstract

Marine microalgae sequester as much CO₂ into carbohydrates as terrestrial plants. Polymeric carbohydrates (i.e., glycans) provide carbon for heterotrophic organisms and constitute a carbon sink in the global oceans. The quantitative contributions of different algal glycans to cycling and sequestration of carbon remain unknown, partly because of the analytical challenge to quantify glycans in complex biological matrices. Here, we quantified a glycan structural type using a recently developed biocatalytic strategy, which involves laminarinase enzymes that specifically cleave the algal glycan laminarin into readily analyzable fragments. We measured laminarin along transects in the Arctic, Atlantic, and Pacific oceans and during three time series in the North Sea. These data revealed a median of 26 ± 17% laminarin within the particulate organic carbon pool. The observed correlation between chlorophyll and laminarin suggests an annual production of algal laminarin of 12 ± 8 gigatons: that is, approximately three times the annual atmospheric carbon dioxide increase by fossil fuel burning. Moreover, our data revealed that laminarin accounted for up to 50% of organic carbon in sinking diatom-containing particles, thus substantially contributing to carbon export from surface waters. Spatially and temporally variable laminarin concentrations in the sunlit ocean are driven by light availability. Collectively, these observations highlight the prominent ecological role and biogeochemical function of laminarin in oceanic carbon export and energy flow to higher trophic levels.

Keywords: carbon cycle; diatoms; diel cycle; glycans; laminarin.

Fig. 1.

Station and laminarin surface concentration overview. The entire dataset comprised samples from nine different cruises and campaigns indicated by different symbols. The colors represent mean laminarin concentrations from surface samples (max. 50 m water depth). No average value was taken for the hourly sampling during the North Sea 2018 campaign in Norway. The enlarged Arctic region is mapped with a polar stereographic projection of the earth whereas the rest of the map and all other enlarged areas are shown in equirectangular projection. Black lines in the gray landmasses mark country borders. The map was created using QGIS (v.2.18.14) and the Natural Earth free vector and raster map.

Fig. 2.

Laminarin and Chl-a concentrations correlate in a North Sea spring bloom time series, in the Atlantic, and in the Arctic. (A) Laminarin and Chl-a were determined in different size fractions during a phytoplankton spring bloom in the North Sea in 2017. (B) Laminarin was measured in different size fractions along a meridional transect from the North to the South Atlantic. (C) Comparison of laminarin and chlorophyll concentrations in all datasets where Chl-a was measured. Linear regression was applied to the laminarin-to-Chl-a relationship (R² = 0.66; P < 0.001, n = 101). The confidence interval (CI) in gray was calculated at level 0.95.

Fig. 3.

Laminarin is a substantial component of particulate organic carbon in diverse oceanic regions. (A) The overview scatter plot comprises all regions where POC was measured. (B) The box plot depicts each individual dataset against the overall median value of Laminarin C:POC. Significant deviations from the overall median and its standard deviation (SD) in gray were tested using the Kruskal–Wallis test (***P < 0.001; *P < 0.05; ns, not significant).

Fig. 4.

Diel-laminarin-cycling in the particulate organic carbon pool. (A) The scatter plot depicts the dataset of laminarin carbon per POC (LamC:POC) in % against the time of day. The gray area marks the time of sunrise and sunset. The sampling took place in spring 2018 during 3 d in the Raunefjorden near Bergen, Norway. On day 3, the sampling was conducted every hour for 24 h. The Inset shows a representative photograph of chain-forming diatoms that dominated the algal bloom. (B) ¹H NMR spectra from two time points at 11:00 (green) and 21:05 (purple) showing the anomeric H-1 doublet of the backbone chain (BC) and H-6 (5 mg⋅mL⁻¹ in D₂O recorded at 600.2 MHz, 313 K, spectra normalized on the area of the ISTD). (C) ¹³C NMR spectrum of the 21:05 sample (250 mg⋅mL⁻¹ in D₂O recorded at 150.94 MHz, 313 K). POC filters were extracted with water at 60 °C. NRT(SRT), (second next to) nonreducing terminus.

Fig. 5.

Net primary production (NPP) pools of carbon after Field et al. (1). Shown are major biological contributors from terrestrial and marine sources, normalized to 400 equal squares, each depicting ∼0.27 gigatons of carbon, which is annually being fixed by primary production; 12 ± 8% of the global carbon production is deposited in the form of the microalgal storage compound laminarin.