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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. 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.