Metagenomic analysis reveals genetic coupling between TonB-dependent transporters and extracellular enzymes in coastal bacterial communities.

Marine heterotrophic prokaryotes initially release extracellular enzymes to cleave large organic molecules and then take up ambient substrates via transporters. Given the direct influence of extracellular enzymes on nutrient availability, understanding their diversity and dynamics is crucial in comprehending microbial interactions and organic matter cycling in aquatic ecosystems. In this study, metagenomics was employed to investigate the functional diversity and dynamics of extracellular enzymes and transporters in coastal waters over a 22-day period. The metagenome-derived gene pool of organic matter-degrading secretory enzymes and transporters was primarily contributed by three major bacterial classes. Bacteroidota were the primary contributors to the gene pool of secretory carbohydrate-active enzymes (CAZymes), whereas Gammaproteobacteria contribute more to secretory peptidases and TonB-dependent transporters (TBDTs), and Alphaproteobacteria to ATP-binding cassette (ABC) transporters. The distinct substrate targets of the enzymes and transporters combined with the unique dynamics of these taxa across depth layers suggest that organic matter degradation and uptake machinery played a role in ecological niche partitioning. At the community level, the abundance of TBDT genes was more positively correlated with extracellular enzymes than ABC transporters. To further explore taxon-specific differences, we reconstructed 163 bacterial and archaeal metagenome-assembled genomes (MAGs). Correlation patterns at the MAG level varied across taxa: Bacteroidota MAGs exhibited significant positive correlations between TBDTs and extracellular enzymes, whereas Gammaproteobacteria and Alphaproteobacteria MAGs showed weak or no significant correlations. These results suggest the diversity of ecological strategies among marine heterotrophic bacteria and highlight a potential coregulation or functional linkage between extracellular enzymes and TBDTs in the metabolism of marine heterotrophic prokaryotes. Our study advances the understanding of the microbial adaptations driving carbon and nutrient cycling. Supplementary Information: The online version contains supplementary material available at 10.1007/s42995-025-00314-9.