Microbially Driven Organic Carbon Degradation and Nutrient Cycling during Macroalgal Decomposition

The release of labile organic carbon (OC) and nutrients during seasonal macroalgal blooms can undermine blue carbon sequestration in coastal ecosystems. Although marine microorganisms mediate OC degradation during macroalgal decay, the underlying mechanisms remain poorly defined. This study employed an integrated multiomics approach (amplicon sequencing, metagenomics, and metatranscriptomics) to investigate microbial regulation of OC degradation and coupled nutrient cycling in coastal sediments with and without decomposing Sargassaceae. Total carbon in sediments increased by over 33% in the Sargassaceae area. Microbial α-diversity in the Sargassaceae area decreased significantly (p < 0.05), while processes linked to OC degradation, carbohydrate metabolism, nitrate (NO₃⁻) reduction, inorganic phosphorus utilization, and sulfur metabolism were significantly upregulated (p < 0.05). Accordingly, gene expression and extracellular hydrolase activities targeting key biopolymers (i.e., cellulose, hemicellulose, starch, and chitin) were significantly upregulated (p < 0.05) in the area with Sargassaceae. Metabolism reconstruction of metagenome-assembled genomes identified Vibrio, Pseudoalteromonas, Alteromonas, and Exiguobacterium_A as primary OC degraders, with genomic capacities enriched in NO₃⁻ reduction and assimilatory sulfate reduction. Key environmental drivers─including the C/N ratio, dissolved organic carbon, total dissolved nitrogen (DON), and NO₃⁻─shaped microbial metabolic activities during macroalgal decomposition. Our finding demonstrates that microbially driven OC degradation is a pivotal process coupled with nutrients cycling, advancing the mechanistic understanding of microbial carbon processing and its biogeochemical linkages during macroalgal decomposition in coastal ecosystems.