Anthropogenically induced shifts in sediment vegetation impact coastal benthic microbiomes

Opportunistic seaweeds of the genus Caulerpa have benefited from human-driven environmental change to expand within coastal lagoons, frequently displacing native seagrasses. In the Mar Menor lagoon (southeastern Spain), Caulerpa prolifera has progressively expanded since the 1970s, coinciding with the decline of the native seagrass Cymodocea nodosa. Sediments colonized by Ca. prolifera are characterized by elevated sulfide concentrations, which are toxic to seagrasses. Because sulfide is microbially produced, these sediment communities likely shape the competition between Ca. prolifera and Cy. nodosa. However, their metabolic potential and activity remain poorly understood. Here, we examined the taxonomic composition and functional capabilities of sediment microbial communities using 12 paired metagenomes and metatranscriptomes from areas dominated by either Ca. prolifera or Cy. nodosa. Caulerpa-associated sediments displayed a higher potential for organic matter degradation and sulfate reduction. Several metagenome-assembled genomes (MAGs) encoded enzymes putatively involved in the degradation of pectin-like polysaccharides characteristic of the Caulerpa cell wall. Comparison of metagenomic and metatranscriptomic data further revealed that the most abundant MAGs were not necessarily the most transcriptionally active. This finding challenges the common assumption that ecological importance is primarily determined by abundance and highlights the potential contribution of less abundant microorganisms to biogeochemical cycling. Further, 97 of the 100 most highly expressed genes lacked functional annotation. Recombinant production and functional characterization of the protein encoded by the most highly expressed gene in the analyzed sediments revealed that it is an enzyme able to breakdown endogenous bacterial peptidoglycan. Collectively, these results underscore the importance of integrating metagenomics and metatranscriptomics with experimental validation to achieve a more comprehensive understanding of microbial functional capabilities, an integration that is still uncommon in the microbial ecology field.