Abstract
Massive influxes of pelagic Sargassum 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 Sargassum degradation, which are still poorly understood. Here, we investigated the microbial degradation of the benthic Sargassum filipendula 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 in vitro degradation timeline. Furthermore, we identified the need for arsenic detoxification pathways in microbes utilizing Sargassum-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 Sargassum polysaccharides and the importance of the in vitro degradation experiment time scale to capture the activities of non-dominant specialists. Our findings elucidate microbial ecosystem dynamics during Sargassum degradation and provide novel insights that can be used to advance the development of biotechnological approaches that leverage renewable Sargassum 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 Sargassum, 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 Sargassum that drives its degradation in nature. To this end, we devised an in-lab degradation assay using Sargassum 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 Sargassum and elucidate microbial ecosystem dynamics during this process. These insights allow the use of renewable Sargassum as a biorefinery feedstock of the future.