Biogeochemistry and ecology of macroalgal-derived dissolved organic carbon
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Biogeochemistry and ecology of macroalgal-derived dissolved organic carbon

Abstract

Marine macroalgae form some of the most productive areas on Earth, but unlike other coastal vegetated ecosystems, macroalgae do not directly store carbon in the benthos, but rather their fixed carbon is exported from their habitats as dissolved organic carbon (DOC) or particulate detritus. While macroalgae are believed to contribute to marine carbon sequestration, there are large uncertainties in the production and fate of macroalgal net primary production (NPP), particularly the fraction that is partitioned into DOC, which is reported to range from <1 to 76%. My work examined the fraction of NPP released as DOC by giant kelp (Macrocystis pyrifera), across gradients in environmental and physiological conditions. The study demonstrated that blade tissue age is an important factor controlling the partitioning of NPP into DOC by giant kelp. Mature blades released on average 2.3% of NPP as DOC with no significant impact of light intensity or tissue nitrogen on percent DOC release. However, when blades entered their senescent phase, DOC production rates increased and became uncoupled from, and sometimes greater than, NPP. The composition of these exudates was investigated by measuring their hydrolyzable sugar content. Significant shifts in the exudate composition between mature and senescent blades were observed. In senescent blades, mannuronic acid was enriched in giant kelp exudates suggesting that structural carbohydrates, such as alginate were being solubilized (i.e. transformed from the particulate phase to the dissolved phase) and that as giant kelp blades senesce, a large fraction of previously fixed biomass is lost as DOC. I also investigated the relationship between the sugar content of giant kelp exudates and the kelp’s microbiome across seasonal and physiological gradients. Significant correlations between the abundance of specific hydrolyzable sugars and the relative abundance of microbial taxa in the kelp microbiome were observed. Mature giant kelp blades were enriched in members of the phylum Planctomycetota that responded positively to carbohydrates rich in fucose and glucosamine. Alternatively, senescent kelp blades were enriched in members of the phylum Bacteroidota that responded positively to carbohydrates rich in mannuronic acid. To validate some of these putative sugar/microbe correlations, a member of the phylum Planctomycetota was isolated to observe its growth on model carbohydrates representative of giant kelp exudates in different seasons and physiological states. Consistent with our previous observations, we found that this isolate was capable of growth on N-acetyl glucosamine and fucoidan, but not alginate. This suggest that the composition of giant kelp exudates may regulate the composition of its microbiome. Lastly, I investigated the bioavailability and photolability of DOC from the pelagic macroalgae Sargassum natans. I found that phenolic compounds are recalcitrant to microbially respiration and may explain the observed recalcitrance of macroalgal DOC in previous studies. However, these compounds are aromatic and absorb UV-light. I demonstrate that these compounds are mostly photooxidized to CO2 when exposed light. These findings provide a more robust understanding of DOC production by macroalgae and highlight its ecological and biogeochemical roles in coastal ocean ecosystems