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Abstract Dinitrogen (N₂) fixation supports marine life through the supply of reactive nitrogen. Recent studies suggest that particle-associated non-cyanobacterial diazotrophs (NCDs) could contribute significantly to N₂fixation contrary to the paradigm of diazotrophy as primarily driven by cyanobacterial genera. We examine the community composition of NCDs associated with suspended, slow, and fast-sinking particles in the North Pacific Subtropical Gyre. Suspended and slow-sinking particles showed a higher abundance of cyanobacterial diazotrophs than fast-sinking particles, while fast-sinking particles showed a higher diversity of NCDs includingMarinobacter,OceanobacterandPseudomonas. Using single-cell mass spectrometry we find that Gammaproteobacteria N₂fixation rates were higher on suspended and slow-sinking particles (up to 67 ± 48.54 fmol N cell⁻¹ d⁻¹), while putative NCDs’ rates were highest on fast-sinking particles (121 ± 22.02 fmol N cell⁻¹ d⁻¹). These rates are comparable to previous diazotrophic cyanobacteria observations, suggesting that particle-associated NCDs may be important contributors to pelagic N₂fixation. 

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. 

The oceanic dissolved organic phosphorus (DOP) pool is mainly composed of P-esters and, to a lesser extent, equally abundant phosphonate and P-anhydride molecules. In phosphate-limited ocean regions, diazotrophs are thought to rely on DOP compounds as an alternative source of phosphorus (P). While both P-esters and phosphonates effectively promote dinitrogen (N 2 ) fixation, the role of P-anhydrides for diazotrophs is unknown. Here we explore the effect of P-anhydrides on N 2 fixation at two stations with contrasting biogeochemical conditions: one located in the Tonga trench volcanic arc region (“volcano,” with low phosphate and high iron concentrations), and the other in the South Pacific Gyre (“gyre,” with moderate phosphate and low iron). We incubated surface seawater with AMP (P-ester), ATP (P-ester and P-anhydride), or 3polyP (P-anhydride) and determined cell-specific N 2 fixation rates, nifH gene abundance, and transcription in Crocosphaera and Trichodesmium . Trichodesmium did not respond to any DOP compounds added, suggesting that they were not P-limited at the volcano station and were outcompeted by the low iron conditions at the gyre station. Conversely, Crocosphaera were numerous at both stations and their specific N 2 fixation rates were stimulated by AMP at the volcano station and slightly by 3polyP at both stations. Heterotrophic bacteria responded to ATP and 3polyP additions similarly at both stations, despite the contrasting phosphate and iron availability. The use of 3polyP by Crocosphaera and heterotrophic bacteria at both low and moderate phosphate concentrations suggests that this compound, in addition to being a source of P, can be used to acquire energy for which both groups compete. P-anhydrides may thus leverage energy restrictions to diazotrophs in the future stratified and nutrient-impoverished ocean.