Disentangling the golden floating rainforest Multi-omics insights into the Sargassum holobiome and its nutrient-driven dynamics

Sargassum natans (genotypes I, VIII) and Sargassum fluitans (genotype III) are holopelagic brown macroalgae that complete their life cycle floating in the Atlantic Ocean. Known as the “golden floating rainforest”, holopelagic Sargassum functions as a biodiversity hotspot and forms a holobiome of the algal host and associated microbiota. Since 2011, holopelagic Sargassum has formed unprecedented accumulations in the North Equatorial Recirculation Region, causing massive coastal strandings. Although the exact drivers remain unclear, nutrient inputs from rivers, Saharan dust, and equatorial upwelling have been implicated. We investigated the genome, transcriptome and microbiome of holopelagic Sargassum and its response to varying environmental nutrient concentrations. De novo genome sequencing of S. fluitans III revealed over 10,000 proteins involved in core cellular functions, with most orthogroups shared with benthic relatives S. fusiforme and S. thunbergii. The microbial community composition differed among Sargassum genotypes, with S. fluitans III hosting the highest microbial diversity. Microbial communities also varied biogeographically and showed high Vibrio abundances in several coastal environments. Sargassum exhibited few differentially expressed genes in response to mixed nutrient additions in ecophysiology experiments, whereas bryozoan epibionts were more strongly affected, upregulating processes related to metabolic and settlement-related processes. A nitrogen/phosphorus limitation experiment indicated potential NP colimitation of Sargassum, while the microbiome responded with shifts in eukaryotic diversity and relative increases in abundances of bacterial epiphytes Schizothrix and Lentilitoribacter, which may themselves experience nutrient limitation. Overall, this thesis provides fundamental insights into holopelagic Sargassum as a holobiome and its versatile responses to nutrient variation in the environment.