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The unicellular diazotrophic cyanobacterium Crocosphaera contributes significantly to fixed nitrogen inputs in the oligotrophic ocean. In the western tropical South Pacific Ocean (WTSP), these diazotrophs abound thanks to the phosphorus-rich waters provided by the South Equatorial Current, and iron provided aeolian and subsurface volcanic activity. East of the WTSP, the South Pacific Gyre (SPG) harbors the most oligotrophic and transparent waters of the world's oceans, where only heterotrophic diazotrophs have been reported before. Here, in the SPG, we detected unexpected accumulation of Crocosphaera at 50 m with peak abundances of 5.26 × 105 nifH gene copies l–1. The abundance of Crocosphaera at 50 m was in the same order of magnitude as those detected westwards in the WTSP and represented 100% of volumetric N2 fixation rates. This accumulation at 50 m was likely due to a deeper penetration of UV light in the clear waters of the SPG being detrimental for Crocosphaera growth and N2 fixation activity. Nutrient and trace metal addition experiments did not induce any significant changes in N2 fixation or Crocosphaera abundance, indicating that this population was not limited by the resources tested and could develop in high numbers despite the oligotrophic conditions. Our findings indicate that the distribution of Crocosphaera can extend into subtropical gyres and further understanding of their controlling factors is needed.

 

Picoplankton populations dominate the planktonic community in the surface oligotrophic ocean. Yet, their strategies in the acquisition and the partitioning of organic and inorganic sources of nitrogen (N) and carbon (C) are poorly described. Here, we measured at the single‐cell level the uptake of dissolved inorganic C (C‐fixation), C‐leucine, N‐leucine, nitrate (NO₃⁻), ammonium (NH₄⁺), and N‐urea in pigmented and nonpigmented picoplankton groups at six low‐N stations in the northwestern Atlantic Ocean. Our study highlights important differences in trophic strategies betweenProchlorococcus,Synechococcus, photosynthetic pico‐eukaryotes, and nonpigmented prokaryotes. Nonpigmented prokaryotes were characterized by high leucine uptake rates, nonsignificant C‐fixation and relatively low NH₄⁺, N‐urea, and NO₃⁻uptake rates. Nonpigmented prokaryotes contributed to 7% ± 3%, 2% ± 2%, and 9% ± 5% of the NH₄⁺, NO₃⁻, and N‐urea community uptake, respectively. In contrast, pigmented groups displayed relatively high C‐fixation rates, NH₄⁺and N‐urea uptake rates, but lower leucine uptake rates than nonpigmented prokaryotes.Synechococcusand photosynthetic pico‐eukaryotes NO₃⁻uptake rates were higher thanProchlorococcusones. Pico‐sized pigmented groups accounted for a significant fraction of the community C‐fixation (63% ± 27%), NH₄⁺uptake (47% ± 27%), NO₃⁻uptake (62% ± 49%), and N‐urea uptake (81% ± 35%). Interestingly,Prochlorococcusand photosynthetic pico‐eukaryotes showed a greater reliance on C‐ and N‐leucine thanSynechococcuson average, suggesting a greater reliance on organic C and N sources. Taken together, our single‐cell results decipher the wide diversity of C and N trophic strategies between and within marine picoplankton groups, but a clear partitioning between pigmented and nonpigmented groups still remains.

 

Nitrogen (N) is a limiting nutrient in vast regions of the world’s oceans, yet the sources of N available to various phytoplankton groups remain poorly understood. In this study, we investigated inorganic carbon (C) fixation rates and nitrate (NO3−), ammonium (NH4+) and urea uptake rates at the single cell level in photosynthetic pico-eukaryotes (PPE) and the cyanobacteria Prochlorococcus and Synechococcus. To that end, we used dual 15N and 13C-labeled incubation assays coupled to flow cytometry cell sorting and nanoSIMS analysis on samples collected in the North Pacific Subtropical Gyre (NPSG) and in the California Current System (CCS). Based on these analyses, we found that photosynthetic growth rates (based on C fixation) of PPE were higher in the CCS than in the NSPG, while the opposite was observed for Prochlorococcus. Reduced forms of N (NH4+ and urea) accounted for the majority of N acquisition for all the groups studied. NO3− represented a reduced fraction of total N uptake in all groups but was higher in PPE (17.4 ± 11.2% on average) than in Prochlorococcus and Synechococcus (4.5 ± 6.5 and 2.9 ± 2.1% on average, respectively). This may in part explain the contrasting biogeography of these picoplankton groups. Moreover, single cell analyses reveal that cell-to-cell heterogeneity within picoplankton groups was significantly greater for NO3− uptake than for C fixation and NH4+ uptake. We hypothesize that cellular heterogeneity in NO3− uptake within groups facilitates adaptation to the fluctuating availability of NO3− in the environment.

 

Considering the reported significant diazotrophic activities in open-ocean regions where primary production is strongly limited by phosphate, we explored the ability of diazotrophs to use other sources of phosphorus to alleviate the phosphate depletion. We tested the actual efficiency of the open-ocean, N 2 -fixer Crocosphaera watsonii to grow on organic phosphorus as the sole P source, and observed how the P source affects the cellular C, N, and P composition. We obtained equivalent growth efficiencies on AMP and DL-α-glycerophosphate as compared with identical cultures grown on phosphate, and survival of the population on phytic acid. Our results show that Crocosphaera cannot use all phosphomonoesters with the same efficiency, but it can grow without phosphate, provided that usable DOP and sufficient light energy are available. Also, results point out that organic phosphorus uptake is not proportional to alkaline phosphatase activity, demonstrating that the latter is not a suitable proxy to estimate DOP-based growth yields of organisms, whether in culture experiments or in the natural environment. The growth parameters obtained, as a function of the P source, will be critical to improve and calibrate mathematical models of diazotrophic growth and the distribution of nitrogen fixation in the global ocean. 

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. The patterns of the large-scale, meso- and submesoscale surface circulation on biogeochemical and biological distributions are examined in the western tropical South Pacific (WTSP) in the context of the OUTPACE cruise (February–April 2015). Multi-disciplinary original in situ observations were achieved along a zonal transect through the WTSP and their analysis was coupled with satellite data. The use of Lagrangian diagnostics allows for the identification of water mass pathways, mesoscale structures, and submesoscale features such as fronts. In particular, we confirmed the existence of a global wind-driven southward circulation of surface waters in the entire WTSP, using a new high-resolution altimetry-derived product, validated by in situ drifters, that includes cyclogeostrophy and Ekman components with geostrophy. The mesoscale activity is shown to be responsible for counter-intuitive water mass trajectories in two subregions: (i) the Coral Sea, with surface exchanges between the North Vanuatu Jet and the North Caledonian Jet, and (ii) around 170°W, with an eastward pathway, whereas a westward general direction dominates. Fronts and small-scale features, detected with finite-size Lyapunov exponents (FSLEs), are correlated with 25% of surface tracer gradients, which reveals the significance of such structures in the generation of submesoscale surface gradients. Additionally, two high-frequency sampling transects of biogeochemical parameters and microorganism abundances demonstrate the influence of fronts in controlling the spatial distribution of bacteria and phytoplankton, and as a consequence the microbial community structure. All circulation scales play an important role that has to be taken into account not only when analysing the data from OUTPACE but also, more generally, for understanding the global distribution of biogeochemical components.

 

Abstract. Heterotrophic prokaryotic production (BP) was studied in the western tropical South Pacific (WTSP) using the leucine technique, revealing spatial and temporal variability within the region. Integrated over the euphotic zone, BP ranged from 58 to 120mg Cm⁻²d⁻¹ within the Melanesian Archipelago, and from 31 to 50mg Cm⁻²d⁻¹ within the western subtropical gyre. The collapse of a bloom was followed during 6 days in the south of Vanuatu using a Lagrangian sampling strategy. During this period, rapid evolution was observed in the three main parameters influencing the metabolic state: BP, primary production (PP) and bacterial growth efficiency. With N₂ fixation being one of the most important fluxes fueling new production, we explored relationships between BP, PP and N₂ fixation rates over the WTSP. The contribution of N₂ fixation rates to bacterial nitrogen demand ranged from 3 to 81%. BP variability was better explained by the variability of N₂ fixation rates than by that of PP in surface waters of the Melanesian Archipelago, which were characterized by N-depleted layers and low DIP turnover times (T_DIP<100h). This is consistent with the fact that nitrogen was often one of the main factors controlling BP on short timescales, as shown using enrichment experiments, followed by dissolved inorganic phosphate (DIP) near the surface and labile organic carbon deeper in the euphotic zone. However, BP was more significantly correlated with PP, but not with N₂ fixation rates where DIP was more available (T_DIP>100h), deeper in the Melanesian Archipelago, or within the entire euphotic zone in the subtropical gyre. The bacterial carbon demand to gross primary production ratio ranged from 0.75 to 3.1. These values are discussed in the framework of various assumptions and conversion factors used to estimate this ratio, including the methodological errors, the daily variability of BP, the bacterial growth efficiency and one bias so far not considered: the ability for Prochlorococcus to assimilate leucine in the dark.

 

Abstract. We assessed the influence of the marine diazotrophic cyanobacterium Trichodesmium on the bio-optical properties of western tropical South Pacific (WTSP) waters (18–22°S, 160°E–160°W) during the February–March 2015 OUTPACE cruise. We performed measurements of backscattering and absorption coefficients, irradiance, and radiance in the euphotic zone with a Satlantic MicroPro free-fall profiler and took Underwater Vision Profiler 5 (UPV5) pictures for counting the largest Trichodesmium spp. colonies. Pigment concentrations were determined by fluorimetry and high-performance liquid chromatography and picoplankton abundance by flow cytometry. Trichome concentration was estimated from pigment algorithms and validated by surface visual counts. The abundance of large colonies counted by the UVP5 (maximum 7093coloniesm⁻³) was well correlated to the trichome concentrations (maximum 2093trichomesL⁻¹) with an aggregation factor of 600. In the Melanesian archipelago, a maximum of 4715trichomesL⁻¹ was enumerated in pump samples (3.2m) at 20°S,16730°E. High Trichodesmium abundance was always associated with absorption peaks of mycosporine-like amino acids (330, 360nm) and high particulate backscattering, but not with high Chl a fluorescence or blue particulate absorption (440nm). Along the west-to-east transect, Trichodesmium together with Prochlorococcus represented the major part of total chlorophyll concentration; the contribution of other groups were relatively small or negligible. The Trichodesmium contribution to total chlorophyll concentration was the highest in the Melanesian archipelago around New Caledonia and Vanuatu (60%), progressively decreased to the vicinity of the islands of Fiji (30%), and reached a minimum in the South Pacific Gyre where Prochlorococcus dominated chlorophyll concentration. The contribution of Trichodesmium to zeaxanthin was respectively 50, 40 and 20% for these regions. During the OUTPACE cruise, the relationship between normalized water-leaving radiance (nL_w) in the ultraviolet and visible and chlorophyll concentration was similar to that found during the BIOSOPE cruise in the eastern tropical Pacific. Principal component analysis (PCA) of OUTPACE data showed that nL_w at 305, 325, 340, 380, 412 and 440nm was strongly correlated to chlorophyll and zeaxanthin, while nL_w at 490 and 565nm exhibited lower correlations. These results, as well as differences in the PCA of BIOSOPE data, indicated that nL_w variability in the greenish blue and yellowish green during OUTPACE was influenced by other variables associated with Trichodesmium presence, such as backscattering coefficient, phycoerythrin fluorescence and/or zeaxanthin absorption, suggesting that Trichodesmium detection should involve examination of nL_w in this spectral domain.

 

Abstract. The western tropical South Pacific (WTSP) Ocean has been recognized as a global hot spot of dinitrogen (N₂) fixation. Here, as in other marine environments across the oceans, N₂ fixation studies have focused on the sunlit layer. However, studies have confirmed the importance of aphotic N₂ fixation activity, although until now only one had been performed in the WTSP. In order to increase our knowledge of aphotic N₂ fixation in the WTSP, we measured N₂ fixation rates and identified diazotrophic phylotypes in the mesopelagic layer along a transect spanning from New Caledonia to French Polynesia. Because non-cyanobacterial diazotrophs presumably need external dissolved organic matter (DOM) sources for their nutrition, we also identified DOM compounds using Fourier transform ion cyclotron resonance mass spectrometry (FTICRMS) with the aim of searching for relationships between the composition of DOM and non-cyanobacterial N₂ fixation in the aphotic ocean. N₂ fixation rates were low (average 0.63±0.07nmolNL⁻¹d⁻¹) but consistently detected across all depths and stations, representing ∼ 6–88% of photic N₂ fixation. N₂ fixation rates were not significantly correlated with DOM compounds. The analysis of nifH gene amplicons revealed a wide diversity of non-cyanobacterial diazotrophs, mostly matching clusters 1 and 3. Interestingly, a distinct phylotype from the major nifH subcluster 1G dominated at 650dbar, coinciding with the oxygenated Subantarctic Mode Water (SAMW). This consistent pattern suggests that the distribution of aphotic diazotroph communities is to some extent controlled by water mass structure. While the data available are still too scarce to elucidate the distribution and controls of mesopelagic non-cyanobacterial diazotrophs in the WTSP, their prevalence in the mesopelagic layer and the consistent detection of active N₂ fixation activity at all depths sampled during our study suggest that aphotic N₂ fixation may contribute significantly to fixed nitrogen inputs in this area and/or areas downstream of water mass circulation.