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Massive influxes of pelagic <i>Sargassum</i> spp. across the tropical Atlantic and Caribbean regions have created urgent ecological and economic challenges that need to be addressed to stabilize local ecosystems. Use of this abundant biomass feedstock resource for biorefining and bioproducts manufacturing is a promising avenue, but this goal requires elucidating the microbial processes that regulate <i>Sargassum</i> degradation, which are still poorly understood. Here, we investigated the microbial degradation of the benthic <i>Sargassum filipendula</i> by native microbiota using multi-omics approaches. Metagenomic and meta-transcriptomic analyses identified diverse carbohydrate-active enzymes (CAZymes), including alginate lyases, fucoidanases, and cellulases, that were differentially expressed over the course of the <i>in vitro</i> degradation timeline. Furthermore, we identified the need for arsenic detoxification pathways in microbes utilizing <i>Sargassum</i>-derived substrates. We observed a suite of factors influencing microbial dynamics, including prokaryotic competition, arsenic detoxification, viruses, and substrate availability. Lineages potentially capable of degrading recalcitrant polysaccharides such as fucoidan appeared to be rapidly outcompeted by other bacteria that utilized simpler substrates like mannitol. These results highlight the metabolic potential of native marine microbial communities to degrade complex <i>Sargassum</i> polysaccharides and the importance of the <i>in vitro</i> degradation experiment time scale to capture the activities of non-dominant specialists. Our findings elucidate microbial ecosystem dynamics during <i>Sargassum</i> degradation and provide novel insights that can be used to advance the development of biotechnological approaches that leverage renewable <i>Sargassum</i> biomass as a biorefinery feedstock of the future.IMPORTANCEThis work addresses a crisis in the tropical Atlantic and Caribbean regions, the massive population growth and stranding of the floating brown seaweed <i>Sargassum</i>, which is wreaking havoc on ecosystems and fouling beaches vital to local tourism. One solution to this problem is to utilize the seaweed as feedstock to generate useful bioproducts. This approach requires characterizing the microbiome of <i>Sargassum</i> that drives its degradation in nature. To this end, we devised an in-lab degradation assay using <i>Sargassum</i> and identified a variety of carbohydrate-active enzymes, including alginate lyases, fucoidanases, and cellulases which break down seaweed cell wall polysaccharides. We also find that microbes compete in the closed reactors, with diversity being reduced over time. These results highlight the metabolic potential of native marine microbial communities to degrade <i>Sargassum</i> and elucidate microbial ecosystem dynamics during this process. These insights allow the use of renewable <i>Sargassum</i> as a biorefinery feedstock of the future.