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Abstract Dinitrogen (N₂) fixation by diazotrophs supports ocean productivity. Diazotrophs include photoautotrophic cyanobacteria, non-cyanobacterial diazotrophs (NCDs) and the recently discovered N2-fixing haptophyte. While NCDs are ubiquitous in the ocean, their ecology and metabolism remain largely unknown. Unlike cyanobacterial diazotrophs and the haptophyte, NCDs are primarily heterotrophic and depend on dissolved organic matter (DOM) for carbon and energy. However, conventional DOM amendment incubations do not allow discerning how different diazotrophs use DOM molecules, limiting our knowledge on DOM-diazotroph interactions. To identify diazotrophs using DOM, we amended North Pacific microbial communities with 13C-labeled DOM from phytoplankton cultures that was molecularly characterized, revealing the dominance of nitrogen-rich compounds. After DOM additions, we observed a community shift from cyanobacterial diazotrophs like Crocosphaera and Trichodesmium to NCDs at stations where the N2-fixing haptophyte abundance was relatively low. Through DNA stable isotope probing and gene sequencing, we identified diverse diazotrophs capable of taking up DOM. Our findings highlight unexpected DOM uptake by the haptophyte’s nitroplast, changes in community structure, and previously unrecognized osmotrophic behavior in NCDs, shaped by local biogeochemical conditions. 

ABSTRACT Seaweeds harbor a rich diversity of bacteria, providing them with metabolic resources and a surface for attachment and biofilm development. The host’s unique environment potentially shapes the bacterial genomes and promotes adaptations for a symbiotic lifestyle. To investigate whether the genomes of seaweed-associated bacteria are genetically and metabolically distinct from their close free-living relatives in seawater, we compared both the seaweed-associated and free-living counterparts of 72 bacterial genera across 16 seaweed hosts using whole-genome sequences or high-quality metagenome-assembled genomes. While taxonomic affiliation strongly influenced genome characteristics such as GC content, gene number, and size, host association had a lower effect overall. A reduced genome size was suggested only inNereocystis luetkeana-associated microbes, while onlyAscophyllum nodosum-associated bacteria had an increased GC content. Metabolic adaptations were indicated from the genomes of seaweed-associated bacteria, including enriched pathways for B vitamin production, complex carbohydrate utilization, and amino acid biosynthesis. In particular,Flavobacteriiashowed the most pronounced differences between host-associated and free-living strains. We further hypothesized that bacteria associated with seaweed might have evolved to complement their host’s metabolism and tested this inference by analyzing the genomes of both the seaweedEctocarpus subulatusand its 28 bacterial associates but found no evidence for such complementarity. Our analyses of 72 paired bacterial genomes highlighted significant metabolic differences in seaweed-associated strains with implications for carbon, nitrogen, and sulfur cycling in the coastal ocean. IMPORTANCEWe hypothesized that the unique environment of seaweeds in coastal oceans shapes bacterial genomes and promotes a symbiotic lifestyle. We compared the genomes of bacteria isolated from seaweed with bacteria from the same genus found free-living in seawater. For genome features that included the number of genes, the size of the genome, and the GC content, taxonomy was of greater importance than bacterial lifestyle. When we compared metabolic abilities, we again found a strong effect of taxonomy in determining metabolism. Although several metabolic pathways differed between free-living and host-associated bacteria, this was especially prominent forFlavobacteriiain the phylumBacteroidota. Notably, bacteria living on seaweeds had an increased occurrence of genes for B vitamin synthesis, complex carbohydrate use, and nitrogen uptake, indicating that bacterial genomes reflect both their evolutionary history and the current environment they inhabit.