Metagenomic insights into microbial mediation of Caulerpa prolifera invasion in a coastal lagoon

Invasive 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 Caulerpa are characterized by elevated sulfide concentrations, which are toxic to seagrasses, suggesting that sediment microbial communities may mediate competitive interactions between these macrophytes. However, the underlying microbial communities and metabolic potential remain poorly understood. Here, we characterized 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 related to 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. Remarkably, the most highly expressed gene in Caulerpa-dominated sediments belonged to a Gammaproteobacteria MAG but lacked functional annotation based on in silico analyses. Recombinant production and functional characterization revealed that the enzyme encoded by this gene is able to breakdown bacterial peptidoglycan, due to endopeptidase or amidase activity. This result highlights the need to integrate 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. Overall, our findings provide mechanistic insight into the microbially mediated displacement of native seagrasses by Ca. prolifera in coastal lagoon ecosystems.