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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 Vitamin B1 (thiamin, B1) is an essential micronutrient for cells, yet intriguingly in aquatic systems most bacterioplankton are unable to synthesize it de novo (auxotrophy), requiring an exogenous source. Cycling of this valuable metabolite in aquatic systems has not been fully investigated and vitamers (B1-related compounds) have only begun to be measured and incorporated into the B1 cycle. Here, we identify potential key producers and consumers of B1 and gain new insights into the dynamics of B1 cycling through measurements of B1 and vitamers (HMP: 4-amino-5-hydroxymethyl-2-methylpyrimidine, HET: 4-methyl-5-thiazoleethanol, FAMP: N-formyl-4-amino-5-aminomethyl-2-methylpyrimidine) in the particulate and dissolved pool in a temperate coastal system. Dissolved B1 was not the primary limiting nutrient for bacterial production and was relatively stable across seasons with concentrations ranging from 74–117 pM, indicating a balance of supply and demand. However, vitamer concentration changed markedly with season as did transcripts related to vitamer salvage and transport suggesting use of vitamers by certain bacterioplankton, e.g. Pelagibacterales. Genomic and transcriptomic analyses showed that up to 78% of the bacterioplankton taxa were B1 auxotrophs. Notably, de novo B1 production was restricted to a few abundant bacterioplankton (e.g. Vulcanococcus, BACL14 (Burkholderiales), Verrucomicrobiales) across seasons. In summer, abundant picocyanobacteria were important putative B1 sources, based on transcriptional activity, leading to an increase in the B1 pool. Our results provide a new dynamic view of the players and processes involved in B1 cycling over time in coastal waters, and identify specific priority populations and processes for future study. 

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. 

Abstract The photosynthetic cyanobacterium Trichodesmium is widely distributed in the surface low latitude ocean where it contributes significantly to N2 fixation and primary productivity. Previous studies found nifH genes and intact Trichodesmium colonies in the sunlight-deprived meso- and bathypelagic layers of the ocean (200–4000 m depth). Yet, the ability of Trichodesmium to fix N2 in the dark ocean has not been explored. We performed 15N2 incubations in sediment traps at 170, 270 and 1000 m at two locations in the South Pacific. Sinking Trichodesmium colonies fixed N2 at similar rates than previously observed in the surface ocean (36–214 fmol N cell−1 d−1). This activity accounted for 40 ± 28% of the bulk N2 fixation rates measured in the traps, indicating that other diazotrophs were also active in the mesopelagic zone. Accordingly, cDNA nifH amplicon sequencing revealed that while Trichodesmium accounted for most of the expressed nifH genes in the traps, other diazotrophs such as Chlorobium and Deltaproteobacteria were also active. Laboratory experiments simulating mesopelagic conditions confirmed that increasing hydrostatic pressure and decreasing temperature reduced but did not completely inhibit N2 fixation in Trichodesmium. Finally, using a cell metabolism model we predict that Trichodesmium uses photosynthesis-derived stored carbon to sustain N2 fixation while sinking into the mesopelagic. We conclude that sinking Trichodesmium provides ammonium, dissolved organic matter and biomass to mesopelagic prokaryotes. 

ABSTRACT Mixotrophy, the combination of heterotrophic and autotrophic nutrition modes, is emerging as the rule rather than the exception in marine photosynthetic plankton. Trichodesmium, a prominent diazotroph ubiquitous in the (sub)tropical oceans, is generally considered to obtain energy via autotrophy. While the ability of Trichodesmium to use dissolved organic phosphorus when deprived of inorganic phosphorus sources is well known, the extent to which this important cyanobacterium may benefit from other dissolved organic matter (DOM) resources is unknown. Here we provide evidence of carbon-, nitrogen- and phosphorus-rich DOM molecules enhancing N2 fixation rates and nifH gene expression in natural Trichodesmium colonies collected at two stations in the western tropical South Pacific. Sampling at a third station located in the oligotrophic South Pacific Gyre revealed no Trichodesmium but showed presence of UCYN-B, although no nifH expression was detected. Our results suggest that Trichodesmium behaves mixotrophically in response to certain environmental conditions, providing them with metabolic plasticity and adding up to the view that mixotrophy is widespread among marine microbes. 

Abstract. Marine diazotrophs convert dinitrogen (N2) gas intobioavailable nitrogen (N), supporting life in the global ocean. In 2012, thefirst version of the global oceanic diazotroph database (version 1) waspublished. Here, we present an updated version of the database (version 2),significantly increasing the number of in situ diazotrophic measurements from13 565 to 55 286. Data points for N2 fixation rates, diazotrophic cellabundance, and nifH gene copy abundance have increased by 184 %, 86 %, and809 %, respectively. Version 2 includes two new data sheets for the nifH genecopy abundance of non-cyanobacterial diazotrophs and cell-specific N2fixation rates. The measurements of N2 fixation rates approximatelyfollow a log-normal distribution in both version 1 and version 2. However,version 2 considerably extends both the left and right tails of thedistribution. Consequently, when estimating global oceanic N2 fixationrates using the geometric means of different ocean basins, version 1 andversion 2 yield similar rates (43–57 versus 45–63 Tg N yr−1; rangesbased on one geometric standard error). In contrast, when using arithmeticmeans, version 2 suggests a significantly higher rate of 223±30 Tg N yr−1 (mean ± standard error; same hereafter) compared to version 1(74±7 Tg N yr−1). Specifically, substantial rate increases areestimated for the South Pacific Ocean (88±23 versus 20±2 Tg N yr−1), primarily driven by measurements in the southwestern subtropics,and for the North Atlantic Ocean (40±9 versus 10±2 Tg N yr−1). Moreover, version 2 estimates the N2 fixation rate in theIndian Ocean to be 35±14 Tg N yr−1, which could not be estimatedusing version 1 due to limited data availability. Furthermore, a comparisonof N2 fixation rates obtained through different measurement methods atthe same months, locations, and depths reveals that the conventional15N2 bubble method yields lower rates in 69 % cases compared tothe new 15N2 dissolution method. This updated version of thedatabase can facilitate future studies in marine ecology andbiogeochemistry. The database is stored at the Figshare repository(https://doi.org/10.6084/m9.figshare.21677687; Shao etal., 2022).