Seasonal and developmental stage changes in mucilage carbohydrate content shape the kelp microbiome

A large amount of a photoautotroph's fixed carbon is released as dissolved organic matter, from both exudation and solubilized detritus. This dissolved material contributes to a surface mucilage layer that shapes their immediate environment, including the composition of their microbiome. Here we evaluated the microbiome and mucilage carbohydrate composition of <i>Macrocystis pyrifera</i> (giant kelp), a globally distributed foundation species, in response to seasonal nutrient availability and developmental stage. We combine 16S rRNA amplicon analysis of the giant kelp microbiome with carbohydrate monomer analysis of kelp mucilage to examine microbe-mucilage relationships. We found significant differences in the microbiome and mucilage composition between seasons and developmental stages of giant kelp. Higher tissue-nitrogen content in the spring coincided with elevated amounts of glucosamine, a nitrogen-containing sugar, in giant kelp mucilage, while senescence led to the release of mannuronic acid, an alginate indicator. The release of glucosamine and fucose-rich mucilage was correlated with an increase in the relative abundance of bacteria within the Planctomycetota phylum, whereas mannuronic acid-rich mucilage coincided with an increase in the relative abundance of members of the Flavobacteriia and Gammaproteobacteria lineages. We investigated putative carbohydrate-microbe relationships by isolating a member of the Planctomycetota phylum from the surface of giant kelp. Using whole genome analysis and growth assays, we demonstrate that this isolate grows on fucoidan and <i>N-</i>acetyl glucosamine, but not alginate, consistent with the observed relative abundance of this clade in the kelp microbiome in response to variable mucilage carbohydrate content. This suggests a key role of kelp mucilage carbohydrate composition in structuring its microbiome as has been observed for other organisms such as corals and within the human gut.